Reduction ofmouse atherosclerosis by urokinase inhibition or with a limited-spectrummatrix metalloproteinase inhibitor

Cardiovascular Research

Volumn 105, Issue 3, 2015, Pages 372-382

  Hu, Jie Hong ^a   Touch, Phanith ^a   Zhang, Jingwan ^a   Wei, Hao ^a   Liu, Shihui ^b   Lund, Ida K ^c   Høyer Hansen, Gunilla ^c   Dichek, David A ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c FINSEN LABORATORY   (Denmark)

Author keywords

Atherosclerosis; Matrix metalloproteinases; Mouse models; Protease inhibition; Urokinase

Indexed keywords

CHOLESTEROL; COLLAGENASE 3; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; MATRIX METALLOPROTEINASE INHIBITOR; MESSENGER RNA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UROKINASE; XL 784; APOLIPOPROTEIN E; LIPID; MMP13 PROTEIN, MOUSE; SERINE PROTEINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AORTA ROOT; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DISEASE COURSE; ENZYME INHIBITION; FEMALE; INTIMA; MALE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; TRIACYLGLYCEROL BLOOD LEVEL; VASODILATATION; ANIMAL; AORTA; AORTIC DISEASES; ATHEROSCLEROSIS; BLOOD; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; LESIONS AND DEFECTS; MACROPHAGE; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; AORTA; AORTIC DISEASES; APOLIPOPROTEINS E; ATHEROSCLEROSIS; DILATATION, PATHOLOGIC; DISEASE MODELS, ANIMAL; LIPIDS; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE INHIBITORS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; SERINE PROTEINASE INHIBITORS; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84964698090     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv007     Document Type: Article

References (45)

1. Garcia-Touchard A, Henry TD, Sangiorgi G, Spagnoli LG, Mauriello A, Conover C, Schwartz RS. Extracellular proteases in atherosclerosis and restenosis. Arterioscler Thromb Vasc Biol 2005;25:1119-1127.
2. Simon DI, Jain MK. Targeting proteases in atherosclerosis: hitting the nail with the hammer. Circulation 2011;124:2480-2482.
3. Dollery CM, Libby P. Atherosclerosis and proteinase activation. Cardiovasc Res 2006;69: 625-635.
4. Turk B. Targeting proteases: successes, failures and future prospects. Nat Rev Drug Discov 2006;5:785-799.
5. Cozen AE, Moriwaki H, Kremen M, DeYoung MB, Dichek HL, Slezicki KI, Young SG, Veniant M, DichekDA. Macrophage-targeted overexpression of urokinase causes accelerated atherosclerosis, coronary artery occlusions, and premature death. Circulation 2004;109:2129-2135.
6. Fuhrman B. The urokinase system in the pathogenesis of atherosclerosis. Atherosclerosis 2012;222:8-14.
7. Janssens S, Lijnen HR. What has been learned about the cardiovascular effects of matrix metalloproteinases from mouse models? Cardiovasc Res 2006;69:585-594.
8. Williams JM, Zhang J, North P, Lacy S, Yakes M, Dahly-Vernon A, Roman RJ. Evaluation of metalloprotease inhibitors on hypertension and diabetic nephropathy. Am J Physiol Renal Physiol 2011;300:F983-F998.
9. Kremen M, Krishnan R, Emery I, Hu JH, Slezicki K, Wu A, Qian K, Du L, Plawman A, Stempien-Otero A, Dichek DA. Plasminogen mediates the atherogenic effects of macrophage-expressed urokinase and accelerates atherosclerosis in apoe-knockout mice. Proc Natl Acad Sci USA 2008;105:17109-17114.
10. Plow EF, Hoover-Plow J. The functions of plasminogen in cardiovascular disease. Trends Cardiovasc Med 2004;14:180-186.
11. Hu JH, Du L, Chu T, Otsuka G, Dronadula N, Jaffe M, Gill SE, Parks WC, Dichek DA. Overexpression of urokinase by plaque macrophages causes histologic features of plaque rupture and increases vascular mmp activity in aged apo e-null mice. Circulation 2010;121:1637-1644.
12. Newby AC. Matrix metalloproteinase inhibition therapy for vascular diseases. Vascul Pharmacol 2012;56:232-244.
13. Lund IK, Jogi A, Rono B, Rasch MG, Lund LR, Almholt K, Gardsvoll H, Behrendt N, Romer J, Hoyer-Hansen G. Antibody-mediated targeting of the urokinase-type plasminogen activator proteolytic function neutralizes fibrinolysis in vivo. J Biol Chem 2008;283:32506-32515.
14. Farris SD, Hu JH, Krishnan R, Emery I, Chu T, Du L, Kremen M, Dichek HL, Gold E, Ramsey SA, Dichek DA. Mechanisms of urokinase plasminogen activator (UPA)- mediated atherosclerosis: role of the upa receptor and s100a8/a9 proteins. J Biol Chem 2011;286:22665-22677.
15. Liu S, Bugge TH, Leppla SH. Targeting of tumor cells by cell surface urokinase plasminogen activator-dependent anthrax toxin. J Biol Chem 2001;276:17976-17984.
16. Liu S, Aaronson H, Mitola DJ, Leppla SH, Bugge TH. Potent antitumor activity of a urokinase-activated engineered anthrax toxin. Proc Natl Acad Sci USA 2003;100: 657-662.
17. Lund IK, Rasch MG, Ingvarsen S, Pass J, Madsen DH, Engelholm LH, Behrendt N, Hoyer-Hansen G. Inhibitory monoclonal antibodies against mouse proteases raised in gene-deficient mice block proteolytic functions in vivo. Front Pharmacol 2012;3:122.
18. Ennis T, Jin J, Bartlett S, Arif B, Grapperhaus K, Curci JA. Effect of novel limited-spectrum mmpinhibitor xl784 in abdominal aortic aneurysms. J Cardiovasc Pharmacol Ther 2012;17: 417-426.
19. Quillard T, Tesmenitsky Y, Croce K, Travers R, Shvartz E, Koskinas KC, Sukhova GK, Aikawa E, Aikawa M, Libby P. Selective inhibition of matrix metalloproteinase-13 increases collagen content of established mouse atherosclerosis. Arterioscler Thromb Vasc Biol 2011;31:2464-2472.
20. Golovchenko S, Hattori T, Hartmann C, Gebhardt M, Gebhard S, Hess A, Pausch F, Schlund B, von der Mark K. Deletion of beta catenin in hypertrophic growth plate chondrocytes impairs trabecular bone formation. Bone 2013;55:102-112.
21. Krishnan R, Kremen M, Hu JH, Emery I, Farris SD, Slezicki KI, Chu T, Du L, Dichek HL, Dichek DA. Level of macrophage upa expression is an important determinant of atherosclerotic lesion growth in apoe-/- mice. Arterioscler Thromb Vasc Biol 2009;29:1737-1744.
22. Rono B, Romer J, Liu S, Bugge TH, Leppla SH, Kristjansen PE. Antitumor efficacy of a urokinase activation-dependent anthrax toxin. Mol Cancer Ther 2006;5:89-96.
23. Carmeliet P, Moons L, Lijnen R, Baes M, Lemaitre V, Tipping P, Drew A, Eeckhout Y, Shapiro S, Lupu F, Collen D. Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation. Nat Genet 1997;17:439-444.
24. Knauper V, Cowell S, Smith B, Lopez-Otin C, O'Shea M, Morris H, Zardi L, Murphy G. The role of the c-terminal domain of human collagenase-3 (mmp-13) in the activation of procollagenase-3, substrate specificity, and tissue inhibitor of metalloproteinase interaction. J Biol Chem 1997;272:7608-7616.
25. Johnson JL, Fritsche-Danielson R, Behrendt M, Westin-Eriksson A, Wennbo H, Herslof M, Elebring M, George SJ, McPheat WL, Jackson CL. Effect of broad-spectrum matrix metalloproteinase inhibition on atherosclerotic plaque stability. Cardiovasc Res 2006;71:586-595.
26. Johnson JL, Devel L, Czarny B, George SJ, Jackson CL, Rogakos V, Beau F, Yiotakis A, Newby AC, Dive V. A selective matrix metalloproteinase-12 inhibitor retards atherosclerotic plaque development in apolipoprotein e-knockout mice. Arterioscler Thromb Vasc Biol 2011;31:528-535.
27. Arribas J, Esselens C. Adam17 as a therapeutic target in multiple diseases. Curr Pharm Des 2009;15:2319-2335.
28. Abboud H, Liljenquist J, Blumenthal S, Ervin W, Rendell M, Aggarwal SK, Mitchell B, Wiliams M. Effect of protease inhibition by xl784 in patients with diabetic nephropathy. J. Am. Soc. Nephrol. 2007;18:329A (abstract).
29. Das R, Ganapathy S, Mahabeleshwar GH, Drumm C, Febbraio M, Jain MK, Plow EF. Macrophage gene expression and foam cell formation are regulated by plasminogen. Circulation 2013;127:1209-1218.
30. Lyons RM, Gentry LE, Purchio AF, Moses HL. Mechanism of activation of latent recombinant transforming growth factor b1 by plasmin. J Cell Biol 1990;110:1361-1367.
31. Klein T, Bischoff R. Physiology and pathophysiology of matrix metalloproteases. Amino Acids 2011;41:271-290.
32. Van Hul M, Bauters D, Lijnen RH. Differential effects of a gelatinase inhibitor on adipocyte differentiation and adipose tissue development. Clin Exp Pharmacol Physiol 2013;40: 689-697.
33. Morikawa T, Toyama T, Kudo N, Kawashima Y. Reducing effect of matrix metalloproteinase inhibitors on serum triacylglycerol in streptozotocin-induced diabetic rats and zucker fa/fa rats. Biol Pharm Bull 2007;30:1461-1467.
34. Goldberg IJ, Eckel RH, McPherson R. Triglycerides and heart disease: still a hypothesis? Arterioscler. Thromb Vasc Biol 2011;31:1716-1725.
35. Di Angelantonio E, Sarwar N, Perry P, Kaptoge S, Ray KK, Thompson A, Wood AM, Lewington S, Sattar N, Packard CJ, Collins R, Thompson SG, Danesh J. Major lipids, apolipoproteins, and risk of vascular disease. JAMA 2009;302:1993-2000.
36. Semenkovich CF, Coleman T, Daugherty A. Effects of heterozygous lipoprotein lipase deficiency on diet-induced atherosclerosis in mice. J Lipid Res 1998;39:1141-1151.
37. Calleja L, Paris MA, Paul A, Vilella E, Joven J, Jimenez A, Beltran G, Uceda M, Maeda N, Osada J. Low-cholesterol and high-fat diets reduce atherosclerotic lesion development in apoe-knockout mice. Arterioscler Thromb Vasc Biol 1999;19:2368-2375.
38. Xiao Q, Danton MJS, Witte DP, Kowala MC, Valentine MT, Bugge TH, Degen JL. Plasminogen deficiency accelerates vessel wall disease in mice predisposed to atherosclerosis. Proc Natl Acad Sci USA 1997;94:10335-10340.
39. Netzel-Arnett S, Mitola DJ, Yamada SS, Chrysovergis K, Holmbeck K, Birkedal- Hansen H, Bugge TH. Collagen dissolution by keratinocytes requires cell surface plasminogen activation and matrix metalloproteinase activity. J Biol Chem 2002;277: 45154-45161.
40. Nakamura H, Sato G, Hirata A, Yamamoto T. Immunolocalization of matrix metalloproteinase-13 on bone surface under osteoclasts in rat tibia. Bone 2004;34: 48-56.
41. Knight CG, Willenbrock F, Murphy G. A novel coumarin-labelled peptide for sensitive continuous assays of the matrix metalloproteinases. FEBS Lett 1992;296:263-266.
42. Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G. Biochemical characterization of human collagenase-3. J Biol Chem 1996;271:1544-1550.
43. 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.
44. Quillard T, Araujo HA, 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.
45. Engelholm LH, Nielsen BS, Netzel-Arnett S, Solberg H, Chen XD, Lopez Garcia JM, Lopez-Otin C, Young MF, Birkedal-Hansen H, Dano K, Lund LR, Behrendt N, Bugge TH. The urokinase plasminogen activator receptor-associated protein/endo180 is coexpressed with its interaction partners urokinase plasminogen activator receptor and matrix metalloprotease-13 during osteogenesis. Lab Invest 2001;81:1403-1414.