Impact of matrix metalloproteinases on atherosclerosis

Current Drug Targets

Volumn 15, Issue 4, 2014, Pages 442-453

  Lin, Juntang ^a,b   Kakkar, Vijay ^c   Lu, Xinjie ^a,c  

^a XINXIANG MEDICAL UNIVERSITY   (China)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c THROMBOSIS RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Atherosclerosis; Inflammation; Knockout mice; Macrophage; Matrix metalloproteinases

Indexed keywords

ACIPIMOX; ANDROSTANOLONE; ATORVASTATIN; BONE MORPHOGENETIC PROTEIN 2; C REACTIVE PROTEIN; COLLAGENASE 3; DAPORINAD; GELATINASE A; GELATINASE B; HEMOPEXIN; ICOSAPENTAENOIC ACID; INTERSTITIAL COLLAGENASE; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE INHIBITOR; MELATONIN; NEUTROPHIL COLLAGENASE; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE; STROMELYSIN; STROMELYSIN 2; TUMOR NECROSIS FACTOR ALPHA;

ACUTE HEART INFARCTION; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; HINGE REGION; HUMAN; HUMORAL IMMUNITY; INFLAMMATION; MACROPHAGE; NONHUMAN; REVIEW; SUDDEN CARDIAC DEATH; UNSTABLE ANGINA PECTORIS;

ANIMALS; ATHEROSCLEROSIS; CATALYTIC DOMAIN; HUMANS; MATRIX METALLOPROTEINASES; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 84896386552     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/1389450115666140211115805     Document Type: Review

References (142)

1. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol 2011; 12: 204-12.
2. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature 2011; 473: 317-25.
3. Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 2011; 17: 1410-22.
4. Schoenhagen P, McErlean ES, Nissen SE. The vulnerable coronary plaque. J Cardiovasc Nurs 2000; 15: 1-12.
5. Wu YW, Kao HL, Chen MF, et al. Characterization of plaques using 18F-FDG PET/CT in patients with carotid atherosclerosis and correlation with matrix metalloproteinase-1. J Nucl Med 2007; 48: 227-33.
6. Underhill HR, Hatsukami TS, Cai J, et al. A noninvasive imaging approach to assess plaque severity: the carotid atherosclerosis score. Am J Neuroradiol 2010; 31: 1068-75.
7. Libby P, Ridker PM. Inflammation and Atherothrombosis: From Population Biology and Bench Research to Clinical Practice, JACC 2006; 48: A33-A46.
8. Shah PK, Galis ZS. Matrix metalloproteinase hypothesis of plaque rupture: players keep piling up but questions remain. Circulation 2001; 104: 1878-80.
9. Cossins J, Dudgeon TJ, Catlin G, et al. Identification of MMP-18, a putative novel human matrix metalloproteinase. Biochem Biophys Res Commun 1996; 228: 494-8.
10. Marchenko GN, Marchenko ND, Strongin AY. The structure and regulation of the human and mouse matrix metalloproteinase-21 gene and protein. Biochem J 2003; 372: 503-15.
11. Pei D, Kang T, Qi H. Cysteine array matrix metalloproteinase (CAMMP)/ MMP-23 is a type II transmembrane matrix metalloproteinase regulated by a single cleavage for both secretion and activation. J Biol Chem 2000; 275: 33988-97.
12. Ohnishi J, Ohnishi E, Jin M, et al. Cloning and characterization of a rat ortholog of MMP-23 (matrix metalloproteinase-23), a unique type of membrane-anchored matrix metalloproteinase and conditioned switching of its expression during the ovarian follicular development. Mol Endocrinol 2001; 15: 747-64.
13. Gururajan R, Lahti JM, Grenet J, et al. Duplication of a genomic region containing the Cdc2L1-2 and MMP21-22 genes on human chromosome 1p36.3 and their linkage to D1Z2. Genome Res 1998; 8: 929-39.
14. Parks WC, Wilson CL, López-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004; 4: 617-29.
15. Trexler M, Briknarová K, Gehrmann M, et al. Peptide ligands for the fibronectin type II modules of matrix metalloproteinase 2 (MMP-2). J Biol Chem 2003; 278: 12241-6.
16. Morgunova E, Tuuttila A, Bergmann U, et al. Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. Science 1999; 284: 1667-70.
17. Osenkowski P, Meroueh SO, Pavel D, et al. Mutational and structural analyses of the hinge region of membrane type 1-matrix metalloproteinase and enzyme processing. J Biol Chem 2005; 280: 26160-8.
18. Tolosano E, Altruda F. Hemopexin: structure, function, and regulation. DNA Cell Biol 2002; 21: 297-306.
19. Hvidberg V, Maniecki MB, Jacobsen C, et al. Identification of the receptor scavenging hemopexin-heme complexes. Blood 2005; 106: 2572-9.
20. Das S, Mandal M, Chakraborti T, et al. Structure and evolutionary aspects of matrix metalloproteinases: a brief overview. Mol Cell Biochem 2003; 253: 31-40.
21. Stura EA, Visse R, Cuniasse P, et al. Crystal structure of fulllength human collagenase 3 (MMP-13) with peptides in the active site defines exosites in the catalytic domain. FASEB J. 2013; 27: 4395-405.
22. Gomis-Rüth FX, Gohlke U, Betz M, et al. The helping hand of collagenase-3 (MMP-13): 2.7 A crystal structure of its C-terminal hemopexin-like domain. J Mol Biol 1996; 264: 556-66.
23. Tochowicz A, Goettig P, Evans R, et al. The dimer interface of the membrane type 1 matrix metalloproteinase hemopexin domain: crystal structure and biological functions. J Biol Chem 2011; 286: 7587-600.
24. Brinckerhoff CE, Ruby PL, Austin SD, et al. Molecular cloning of human synovial cell collagenase and selection of a single gene from genomic DNA. J Clin Invest 1987; 79: 542-6.
25. Saffarian S, Collier IE, Marmer BL, et al. Interstitial collagenase is a Brownian ratchet driven by proteolysis of collagen. Science 2004; 306: 108-11.
26. Jeffrey JJ. Interstitial collagenases. In Matrix metalloproteinases. Parks WC and Mecham RP. editors. Academic Press Inc. San Diego, California, USA. 1998; 15-42.
27. Matrisian LM. The matrix-degrading metalloproteinases. Bioessays 1992; 14: 455-63.
28. Morton LF, Barnes MJ. Collagen polymorphism in the normal and diseased blood vessel wall. Investigation of collagens types I, III and V. Atherosclerosis 1982; 42: 41-51.
29. Hanson AN, Bentley JP. Quantitation of type I to type III collagen ratios in small samples of human tendon, blood vessels, and atherosclerotic plaques. Anal Biochem 1983; 130: 32-40.
30. Katsuda S, Okada Y, Minamoto T, et al. Collagens in human atherosclerosis. Immunohistochemical analysis using collagen typespecific antibodies. Arterioscler Thromb 1992; 12: 494-502.
31. Chung L, Shimokawa K, Dinakarpandian D, et al. Identification of the (183)RWTNNFREY(191) region as a critical segment of matrix metalloproteinase 1 for the expression of collagenolytic activity. J Biol Chem 2000; 275: 29610-17.
32. Austin KM, Covic L, Kuliopulos A. Matrix metalloproteases and PAR1 activation. Blood 2013; 121: 431-9.
33. Gearing AJ, Beckett P, Christodoulou M, et al. Matrix metalloproteinases and processing of pro-TNF-alpha. J Leukoc Biol 1995; 57: 774-7.
34. Saunders WB, Bayless KJ, Davis GE. MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices. J Cell Sci 2005; 118: 2325-40.
35. Sukhova GK, Schönbeck U, Rabkin E, et al. Evidence for increased collagenolysis by interstitial collagenases-1 and-3 in vulnerable human atheromatous plaques. Circulation 1999; 99: 2503-9.
36. Galis ZS, Sukhova GK, Lark MW, et al. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest 1994; 94: 2493-503.
37. Newby AC: Metalloproteinase expression in monocytes and macrophages and its relationship to atherosclerotic plaque instability. Arterioscler Thromb Vasc Biol 2008; 28: 2108-14.
38. Richard PD, Davies MJ, Born GVR. Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaques. Lancet 1989; 2: 941-4.
39. McCarthy MJ, Loftus IM, Thompson MM, et al. Angiogenesis and the atherosclerotic carotid plaque: an association between symptomatology] and plaque morphology. J Vasc Surg 1999; 30: 261-8.
40. Lehrke M, Greif M, Broedl UC, et al. MMP-1 serum levels predict coronary atherosclerosis in humans. Cardiovasc Diabetol 2009; 8: 50.
41. Hirohata S, Kusachi S, Murakami M, et al. Time dependent alterations of serum matrix metalloproteinase-1 and metalloproteinase-1 tissue inhibitor after successful reperfusion of acute myocardial infarction. Heart 1997; 78: 278-84.
42. Huang WC, Sala-Newby GB, Susana A, et al. Classical macrophage activation up-regulates several matrix metalloproteinases through mitogen activated protein kinases and nuclear factor-κB. PLoS One 2012; 7: e42507.
43. Ichiki T, Jougasaki M, Setoguchi M, et al. Cardiotrophin-1 stimulates intercellular adhesion molecule-1 and monocyte chemoattractant protein-1 in human aortic endothelial cells. Am J Physiol Heart Circ Physiol. 2008; 294: H750-63.
44. Tokito A, Jougasaki M, Ichiki T, et al. Cardiotrophin-1 induces matrix metalloproteinase-1 in human aortic endothelial cells. PLoS One. 2013; 8: e68801.
45. Li Z, Li L, Zielke HR, et al. Increased expression of 72-kd type IV collagenase (MMP-2) in human aortic atherosclerotic lesions. Am J Pathol 1996; 148: 121-8.
46. Fernández-Robredo P, Sádaba LM, Salinas-Alamán A, et al. Effect of Lutein and Antioxidant Supplementation on VEGF Expression, MMP-2 Activity, and Ultrastructural Alterations in Apolipoprotein E-Deficient Mouse Oxid Med Cell Longev 2013; 2013: 505.
47. Sasaki T, Nakamura K, Sasada K, et al. Matrix metalloproteinase-2 deficiency impairs aortic atherosclerotic calcification in ApoEdeficient mice. Atherosclerosis 2013; 227: 43-50.
48. Kim YH, Lee SJ, Seo KW, et al. PAF enhances MMP-2 production in rat aortic VSMCs via a β-arrestin2-dependent ERK signaling pathway. J Lipid Res. 2013; 54: 2678-86.
49. Caird J, Napoli C, Taggart C, et al. Matrix metalloproteinases 2 and 9 in human atherosclerotic and non-atherosclerotic cerebral aneurysms. Eur J Neurol. 2006; 13: 1098-105.
50. Jeon SB, Chun S, Choi-Kwon S, et al. Biomarkers and location of atherosclerosis: matrix metalloproteinase-2 may be related to intracranial atherosclerosis. Atherosclerosis 2012; 223: 442-7.
51. Yeh JL, Hsu JH, Liang JC, et al. Lercanidipine and labedipinedilol--A attenuate lipopolysaccharide/interferon-γ-induced inflammation in rat vascular smooth muscle cells through inhibition of HMGB1 release and MMP-2, 9 activities. Atherosclerosis 2013; 226: 364-72.
52. Nakaya R, Uzui H, Shimizu H, et al. Pravastatin suppresses the increase in matrix metalloproteinase-2 levels after acute myocardial infarction. Int J Cardiol 2005; 105: 67-73.
53. Tziakas DN, Chalikias GK, Parissis JT, et al. Serum profiles of matrix metalloproteinases and their tissue inhibitor in patients with acute coronary syndromes. The effects of short-term atorvastatin administration. Int J Cardiol 2004; 94: 269-77.
54. Wang KF, Huang PH, Chiang CH, et al. Usefulness of plasma matrix metalloproteinase-9 level in predicting future coronary revascularization in patients after acute myocardial infarction. Coron Artery Dis 2013; 24: 23-8.
55. Oviedo-Orta E, Bermudez-Fajardo A, Karanam S, et al. Comparison of MMP-2 and MMP-9 secretion from T helper 0, 1 and 2 lymphocytes alone and in coculture with macrophages. Immunology 2008; 124: 42-50.
56. Jin F, Jiang S, Yang D, et al. Acipimox attenuates atherosclerosis and enhances plaque stability in ApoE-deficient mice fed a palmitate-rich diet. Biochem Biophys Res Commun 2012; 428: 86-92.
57. Flechtner-Mors M, Jenkinson CP, Alt A, et al. Effects of acipimox on the lipolysis rate in subcutaneous adipose tissue of obese subjects. Diabetes Metab Res Rev. 2001; 17: 387-390.
58. Wågsäter D, Zhu C, Björkegren J, et al. MMP-2 and MMP-9 are prominent matrix metalloproteinases during atherosclerosis development in the Ldlr(-/-)Apob(100/100) mouse. Int J Mol Med. 2011; 28: 247-53.
59. Ishibashi M, Sayers S, D'Armiento JM, et al. TLR3 deficiency protects against collagen degradation and medial destruction in murine atherosclerotic plaques. Atherosclerosis 2013; 229: 52-61.
60. Kumar H, Kawai T, Akira S. Toll-like receptors and innate immunity. Biochem Biophys Res Commun. 2009; 388: 621-5.
61. Henney AM, Wakeley PR, Davies MJ, et al. Localization of stromelysin gene expression in atherosclerotic plaques by in situ hybridization. Proc Natl Acad Sci USA 1991; 88: 8154-8.
62. Silence J, Lupu F, Collen D, et al. Persistence of atherosclerotic plaque but reduced aneurysm formation in mice with stromelysin-1 (MMP-3) gene inactivation. Arterioscler Thromb Vasc Biol 2001; 21: 1440-5.
63. Sherva R, Ford CE, Eckfeldt JH, et al. Pharmacogenetic effect of the stromelysin (MMP3) polymorphism on stroke risk in relation to antihypertensive treatment: the genetics of hypertension associated treatment study. Stroke 2011; 42: 330-5.
64. Fateh-Moghadam S, Htun P, Tomandl B, et al. Hyperresponsiveness of platelets in ischemic stroke. Thromb Haemost. 2007; 97: 974-8.
65. Ghaderian SM, Akbarzadeh Najar R, Tabatabaei Panah AS. Genetic polymorphisms and plasma levels of matrix metalloproteinases and their relationships with developing acute myocardial infarction. Coron Artery Dis 2010; 21: 330-5.
66. Djurić T, Zivković M, Radak D, et al. Association of MMP-3 5A/6A gene polymorphism with susceptibility to carotid atherosclerosis. Clin Biochem 2008; 41: 1326-9.
67. Souslova V, Townsend PA, Mann J, et al. Allele-specific regulation of matrix metalloproteinase-3 gene by transcription factor NFkappaB. PLoS One 2010; 5: e9902.
68. Johnson JL, Dwivedi A, Somerville M, et al. Matrix metalloproteinase (MMP)-3 activates MMP-9 mediated vascular smooth muscle cell migration and neointima formation in mice. Arterioscler Thromb Vasc Biol 2011; 31: e35-44.
69. Hasty KA, Pourmotabbed TF, Goldberg GI, et al. A distinct gene product with homology to other matrix metalloproteinases. J Biol Chem 1990; 265: 11421-4.
70. Nikkari ST, O'Brien KD, Ferguson M, et al. Interstitial collagenase (MMP-1) expression in human carotid atherosclerosis. Circulation 1995; 92: 1393-8.
71. Herman MP, Sukhova GK, Libby P, et al. Expression of neutrophil collagenase (matrix metalloproteinase-8) in human atheroma: a novel collagenolytic pathway suggested by transcriptional profiling. Circulation 2001; 104: 1899-904
72. Turu MM, Krupinski J, Catena E, et al. Intraplaque MMP-8 levels are increased in asymptomatic patients with carotid plaque progression on ultrasound. Atherosclerosis 2006; 187: 161-9.
73. Xiao Q, Zhang F, Lin L, et al. Functional role of matrix metalloproteinase-8 in stem/progenitor cell migration and their recruitment into atherosclerotic lesions. Circ Res 2013; 112: 35-47.
74. Laxton RC, Hu Y, Duchene J, et al. A role of matrix metalloproteinase-8 in atherosclerosis. Circ Res 2009; 105: 921-9.
75. Djurić T, Stanković A, Končar I, et al. Association of MMP-8 promoter gene polymorphisms with carotid atherosclerosis: preliminary study. Atherosclerosis 2011; 219: 67367-8.
76. Chiao YA, Ramirez TA, Zamilpa R, et al. Matrix metalloproteinase-9 deletion attenuates myocardial fibrosis and diastolic dysfunction in ageing mice. Cardiovasc Res 2012; 96: 444-55.
77. Dabek J, Glogowska-Ligus J, Szadorska B. Transcription activity of MMP-2 and MMP-9 metalloproteinase genes and their tissue inhibitor (TIMP-2) in acute coronary syndrome patients. J Postgrad Med 2013; 59: 115-20.
78. Ramos-Fernandez M, Bellolio MF, Stead LG. Matrix metalloproteinase-9 as a marker for acute ischemic stroke: a systematic review. J Stroke Cerebrovasc Dis. 2011; 20: 47-54.
79. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003; 92: 827-39.
80. Zhang B, Ye S, Herrmann SM, et al. Functional polymorphism in the regulatory region of gelatinase B gene in relation to severity of coronary atherosclerosis. Circulation 1999; 99: 1788-94.
81. Pearce E, Tregouet DA, Samnegard A, et al. Haplotype effect of the matrix metalloproteinase-1 gene on risk of myocardial infarction. Circ Res 2005; 97: 1070-6.
82. Aono J, Suzuki J, Iwai M, et al. Deletion of the angiotensin II type 1a receptor prevents atherosclerotic plaque rupture in apolipoprotein E-/-mice. Arterioscler Thromb Vasc Biol 2012; 32: 1453-9.
83. Galis ZS, Johnson C, Godin D, et al. Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling. Circ Res 2002; 91: 852-9.
84. Kuzuya M, Kanda S, Sasaki T, et al. Deficiency of gelatinase A suppresses smooth muscle cell invasion and development of experimental intimal hyperplasia. Circulation 2003; 108: 1375-81.
85. Huang Y, Yin H, Wang J, et al. Aberrant expression of FcγRIIIA (CD16) contributes to the development of atherosclerosis. Gene 2012; 498: 91-5.
86. Sommerville LJ, Kelemen SE, Ellison SP, et al. Increased atherosclerosis and vascular smooth muscle cell activation in AIF-1 transgenic mice fed a high-fat diet. Atherosclerosis 2012; 220: 45-52.
87. Hans CP, Feng Y, Naura AS, et al. Opposing roles of PARP-1 in MMP-9 and TIMP-2 expression and mast cell degranulation in dyslipidemic dilated cardiomyopathy. Cardiovasc Pathol 2011; 20: e57-68.
88. Netherland CD, Pickle TG, Bales A, et al. Cannabinoid receptor type 2 (CB2) deficiency alters atherosclerotic lesion formation in hyperlipidemic Ldlr-null mice. Atherosclerosis 2010; 213: 102-8.
89. Stintzing S, Heuschmann P, Barbera L, et al. Overexpression of MMP9 and tissue factor in unstable carotid plaques associated with Chlamydia pneumoniae, inflammation, and apoptosis. Ann Vasc Surg 2005; 19: 310-9.
90. Rodriguez JA, Orbe J, Martinez de Lizarrondo S, et al. Metalloproteinases and atherothrombosis: MMP-10 mediates vascular remodeling promoted by inflammatory stimuli. Front Biosci 2008; 13: 2916-21.
91. Martínez de Lizarrondo S, Roncal C, Calvayrac O, et al. Synergistic effect of thrombin and CD40 ligand on endothelial matrix metalloproteinase-10 expression and microparticle generation in vitro and in vivo. Arterioscler Thromb Vasc Biol 2012; 32: 1477-87.
92. Montero I, Orbe J, Varo N, 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: 1369-78.
93. Orbe J, Montero I, Rodríguez JA, et al. Independent association of matrix metalloproteinase-10, cardiovascular risk factors and subclinical atherosclerosis. J Thromb Haemost 2007; 5: 91-7.
94. Orbe J, Barrenetxe J, Rodriguez JA, et al. Matrix metalloproteinase-10 effectively reduces infarct size in experimental stroke by enhancing fibrinolysis via a thrombin-activatable fibrinolysis inhibitor-mediated mechanism. Circulation 2011; 124: 2909-19.
95. Banda MJ, Werb Z. Mouse macrophage elastase. Purification and characterization as a metalloproteinase. Biochem J 1981; 193: 589-605.
96. Shapiro SD, Kobayashi DK, Ley TJ. Cloning and characterization of a unique elastolytic metalloproteinase produced by human alveolar macrophages. J Biol Chem 1993; 268: 23824-9.
97. Scholtes VP, Johnson JL, Jenkins N, et al. Carotid atherosclerotic plaque matrix metalloproteinase-12-positive macrophage subpopulation predicts adverse outcome after endarterectomy. J Am Heart Assoc 2012; 1: e001040.
98. Souissi IJ, Billiet L, Cuaz-Pérolin C, et al. Matrix metalloproteinase-12 gene regulation by a PPAR alpha agonist in human monocyte-derived macrophages. Exp Cell Res 2008; 314: 3405-14.
99. Belaaouaj A, Shipley JM, Kobayashi DK, et al. Human macrophage metalloelastase. Genomic organization, chromosomal location, gene linkage, and tissue-specific expression. J Biol Chem 1995; 270: 14568-75.
100. Halpert I, Sires UI, Roby JD, et al. Matrilysin is expressed by lipidladen 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 USA 1996; 93: 9748-53.
101. Johnson JL, Devel L, Czarny B, et al. A selective matrix metalloproteinase-12 inhibitor retards atherosclerotic plaque development in apolipoprotein E-knockout mice. Arterioscler Thromb Vasc Biol 2011; 31: 528-35.
102. Song Y, Xie Y, Liu F, et al. Expression of matrix metalloproteinase-12 in aortic dissection. BMC Cardiovasc Disord 2013; 13: 34.
103. Barascuk N, Genovese F, Larsen L, et al. A MMP derived versican neo-epitope is elevated in plasma from patients with atherosclerotic heart disease. Int J Clin Exp Med 2013; 6: 174-84.
104. Chinetti G, Griglio S, Antonucci M, et al. Activation of proliferator-activated receptors alpha and gamma induces apoptosis of human monocyte-derived macrophages. J Biol Chem 1998; 273: 25573-80.
105. Johnson JL, George SJ, Newby AC, et al. Divergent effects of matrix metalloproteinases 3, 7, 9, and 12 on atherosclerotic plaque stability in mouse brachiocephalic arteries. Proc Natl Acad Sci USA 2005; 102: 15575-80.
106. Fan J, Wang X, Wu L, et al. Macrophage-specific overexpression of human matrix metalloproteinase-12 in transgenic rabbits. Transgenic Res 2004; 13: 261-9.
107. Prescott MF, Sawyer WK, Von Linden-Reed J, et al. Effect of matrix metalloproteinase inhibition on progression of atherosclerosis and aneurysm in LDL receptor-deficient mice overexpressing MMP-3, MMP-12, and MMP-13 and on restenosis in rats after balloon injury. Ann N Y Acad Sci 1999; 878: 179-90.
108. Deguchi JO, Aikawa E, Libby P, et al. Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation 2005; 112: 2708-15.
109. Newby AC. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 2006; 85: 1-31.
110. Quillard T, Tesmenitsky Y, Croce K, et al. Selective inhibition of matrix metalloproteinase-13 increases collagen content of established mouse atherosclerosis. Arterioscler Thromb Vasc Biol. 2011; 31: 2464-72.
111. Chistiakov DA, Sobenin IA, Orekhov AN. Vascular Extracellular Matrix in Atherosclerosis. Cardiol Rev 2013; 21: 270-88.
112. Schneider F, Sukhova GK, Aikawa M, et al. Matrixmetalloproteinase-14 deficiency in bone-marrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques. Circulation 2008; 117: 931-9.
113. Pelisek J, Rudelius M, Zepper P, et al. Multiple biological predictors for vulnerable carotid lesions. Cerebrovasc Dis 2009; 28: 601-10.
114. Morgan AR, Rerkasem K, Gallagher PJ, et al. Differences in matrix metalloproteinase-1 and matrix metalloproteinase-12 transcript levels among carotid atherosclerotic plaques with different histopathological characteristics. Stroke 2004; 35: 1310-5.
115. Tziakas DN, Lazarides MK, Tentes IK, et al. Gelatinases [matrix metalloproteinase-2 (MMP-2) and MMP-9] induce carotid plaque instability but their systemic levels are not predictive of local events. Ann Vasc Surg 2005; 19: 529-33.
116. Furfaro AL, Sanguineti R, Storace D, et al. Metalloproteinases and advanced glycation end products: coupled navigation in atherosclerotic plaque pathophysiology? Exp Clin Endocrinol Diabetes 2012; 120: 586-90.
117. Bicknell CD, Peck D, Alkhamesi NA, et al. Relationship of matrix metalloproteinases and macrophages to embolization during endoluminal carotid interventions. J Endovasc Ther 2004; 11: 483-93.
118. Razuvaev A, Ekstrand J, Folkersen L, et al. Correlations between clinical variables and gene-expression profiles in carotid plaque instability. Eur J Vasc Endovasc Surg 2011; 42: 722-30.
119. Shin IJ, Shon SM, Schellingerhout D, et al. Characterization of partial ligation-induced carotid atherosclerosis model using dualmodality molecular imaging in ApoE knock-out mice. PLoS One. 2013; 8: e73451.
120. Molloy KJ, Thompson MM, Jones JL, et al. Unstable carotid plaques exhibit raised matrix metalloproteinase-8 activity. Circulation 2004; 110: 337-43.
121. Krupinski J, Turu MM, Font MA, et al. Increased tissue factor, MMP-8, and D-dimer expression in diabetic patients with unstable advanced carotid atherosclerosis. Vasc Health Risk Manag 2007; 3: 405-12.
122. Paim LR, Schreiber R, Matos-Souza JR, et al. Oxidized lowdensity lipoprotein, matrix-metalloproteinase-8 and carotid atherosclerosis in spinal cord injured subjects. Atherosclerosis. 2013; 231: 341-5.
123. Loftus IM, Naylor AR, Goodall S, et al. Increased matrix metalloproteinase-9 activity in unstable carotid plaques. A potential role in acute plaque disruption. Stroke 2000; 31: 40-7.
124. Alvarez B, Ruiz C, Chacon P, et al. Serum values of metalloproteinase-2 and metalloproteinase-9 as related to unstable plaque and inflammatory cells in patients with greater than 70% carotid artery stenosis. J Vasc Surg 2004; 40: 469-75.
125. Choi ET, Collins ET, Marine LA, et al. Matrix metalloproteinase-9 modulation by resident arterial cells is responsible for injuryinduced accelerated atherosclerotic plaque development in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25: 1020-5.
126. Kunte H, Kunte G, Busch MA, et al. Differences in carotid plaque content of macrophages, T cells and MMP-9 between patients with embolic and hemodynamic cerebral ischemia due to symptomatic carotid stenosis. Atherosclerosis 2010; 211: 456-60.
127. Kai H, Ikeda H, Yasukawa H, et al. Peripheral blood levels of matrix metalloproteases-2 and-9 are elevated in patients with acute coronary syndromes. J Am Coll Cardiol 1998; 32: 368-72.
128. Heo SH, Cho CH, Kim HO, et al. Plaque rupture is a determinant of vascular events in carotid artery atherosclerotic disease: involvement of matrix metalloproteinases 2 and 9. J Clin Neurol 2011; 7: 69-76.
129. Brown DL, Hibbs MS, Kearney M, et al. Identification of 92-kD gelatinase in human coronary atherosclerotic lesions: association of active enzyme synthesis with unstable angina. Circulation 1995; 91: 2125-31.
130. Khokha R, Murthy A, Weiss A. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat Rev Immunol. 2013; 13: 649-65.
131. Roycik MD, Myers JS, Newcomer RG, et al. Matrix metalloproteinase inhibition in atherosclerosis and stroke. Curr Mol Med. 2013; 13: 1299-313.
132. Mountain DJ, Freeman BM, Kirkpatrick SS, et al. Androgens regulate MMPs and the cellular processes of intimal hyperplasia. J Surg Res. 2013; 184: 619-27.
133. Gu G, Zhao D, Yin Z, et al. BST-2 binding with cellular MT1-MMP blocks cell growth and migration via decreasing MMP2 activity. J Cell Biochem 2012; 113: 1013-21.
134. Xia Y, Dobaczewski M, Gonzalez-Quesada C, et al. Endogenous thrombospondin 1 protects the pressure-overloaded myocardium by modulating fibroblast phenotype and matrix metabolism. Hypertension 2011; 58: 902-11.
135. Saraf S, Saraf S, Kaur CD, et al. Matrix metalloproteinase enzymes and their naturally derived inhibitors: Novel targets in photocarcinoma therapy. Ageing Res Rev 2013; 13C: 65-74.
136. Kageyama A, Matsui H, Ohta M, et al. Palmitic acid induces osteoblastic differentiation in vascular smooth muscle cells through ACSL3 and NF-κB, novel targets of eicosapentaenoic acid. PLoS One 2013; 8: e68197.
137. Yang HL, Chang HC, Lin SW, et al. Antrodia salmonea inhibits TNF-α-induced angiogenesis and atherogenesis in human endothelial cells through the down-regulation of NF-κB and up-regulation of Nrf2 signaling pathways. J Ethnopharmacol 2014; 151: 394-406.
138. Nencioni A, da Silva RF, Fraga-Silva RA, et al. Nicotinamide phosphoribosyltransferase inhibition reduces intraplaque CXCL1 production and associated neutrophil infiltration in atherosclerotic mice. Thromb Haemost 2014; 111: 308-22.
139. Sun Y, Liu J, Yang B, et al. Inhibitory effect of co-administration of atorvastatin and endothelin-1 receptor antagonist on the progression of atherosclerosis in rabbit. APMIS 2013; [Epub ahead of print].
140. Rudra DS, Pal U, Maiti NC, et al. Melatonin inhibits matrix metalloproteinase-9 activity by binding to its active site. J Pineal Res 2013; 54: 398-405.
141. -/- Mice. Arterioscler Thromb Vasc Biol 2008; 28: 272-7.
142. Wolak T, Sion-Vardi N, Novack V, et al. N-terminal rather than full-length osteopontin or its C-terminal fragment is associated with carotid-plaque inflammation in hypertensive patients. Am J Hypertens 2013; 26: 326-33.