Download PDF
Thromb Haemost 2001; 86(01): 324-333
DOI: 10.1055/s-0037-1616230
Research Article
Schattauer GmbH

Plasmin and Matrix Metalloproteinases in Vascular Remodeling

H. R. Lijnen
1   Center for Molecular and Vascular Biology; University of Leuven, Belgium
› Author Affiliations
Further Information

Publication History

Publication Date:
12 December 2017 (online)

    Permissions and Reprints

Summary

Vascular remodeling, defined as lasting structural changes in the vessel wall in response to hemodynamic stimuli, plays a role in many (patho)physiological processes requiring cell migration and degradation of extracellular matrix (ECM). Two proteolytic systems, the fibrinolytic (plasminogen/plasmin) and matrix metalloproteinase (MMP) systems can degrade most ECM components. The availability of mice models with deficiency of main components of both systems has allowed to study their contribution to vascular remodeling in several biological processes. In mouse models of atherosclerosis, urokinase-mediated plasmin generation plays a role in activation of several macrophage-derived MMPs (MMP-3, -9, -12 and -13), triggering elastolysis and collagenolysis, resulting in media destruction and aneurysm formation. Neointima formation after vascular injury, a process that depends on smooth muscle cell migration, is reduced in mice with plasminogen or urokinase deficiency and enhanced in mice with deficiency of TIMP-1 (type 1 tissue inhibitor of MMPs). Also in allograft transplant arteriosclerosis and in abdominal aortic aneurysm both proteolytic systems contribute to matrix degradation. In a mouse model of myocardial infarction, urokinase deficiency protects totally and MMP-9 deficiency partially against cardiac rupture, but these animals suffer cardiac failure. Thus, the plasminogen/plasmin and MMP systems, in concert, contribute to vascular remodeling in the setting of cardiovascular disease.

Key words

Fibrinolysis - matrix metalloproteinases - vascular remodeling - cardiovascular disease
 

  • References

  • 1 Herity NA, Ward MR, Lo S, Yeung AC. Review: Clinical aspects of vascular remodeling. J Cardiovasc Electrophysiol 1999; 10: 1016-24.
    CrossrefPubMedGoogle Scholar
  • 2 Carmeliet P, Collen D. Development and disease in proteinase-deficient mice: role of the plasminogen, matrix metalloproteinase and coagulation system. Thromb Res 1998; 91: 255-85.
    CrossrefPubMedGoogle Scholar
  • 3 Lijnen HR. Molecular interactions between the plasminogen/plasmin and matrix metalloproteinase systems. Fibrinolysis & Proteolysis 2000; 14: 175-81.
    CrossrefPubMedGoogle Scholar
  • 4 Dickey RP, Hover JF. Ultrasonographic features of uterine blood flow during the first 16 weeks of pregnancy. Hum Reprod 1995; 10: 2448-52.
    CrossrefPubMedGoogle Scholar
  • 5 Lijnen HR, Collen D. Mechanisms of physiological fibrinolysis. Baillière’s Clinical Haematology 1995; 8: 277-90.
    PubMedGoogle Scholar
  • 6 Collen D, Lijnen HR. Basic and clinical aspects of fibrinolysis and thrombolysis. Blood 1991; 78: 3114-24.
    PubMedGoogle Scholar
  • 7 Blasi F. Urokinase and urokinase receptor: A paracrine/autocrine system regulating cell migration and invasiveness. BioEssays 1993; 15: 105-11.
    CrossrefPubMedGoogle Scholar
  • 8 Vassalli JD, Sappino AP, Belin D. The plasminogen activator/plasmin system. J Clin Invest 1991; 88: 1067-72.
    CrossrefPubMedGoogle Scholar
  • 9 Declerck PJ, Juhan-Vague I, Felez J, Wiman B. Pathophysiology of fibrinolysis. J Int Med 1994; 236: 425-32.
    CrossrefPubMedGoogle Scholar
  • 10 Parks WC, Mecham RP. Matrix metalloproteinases. San Diego: Academic Press; 1998
    Google Scholar
  • 11 Birkedal-Hansen H, Moore WG, Bodden MK, Windsor LJ, Birkedal-Hansen B, DeCarlo A, Engler JA. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993; 4: 197-250.
    CrossrefPubMedGoogle Scholar
  • 12 Nagase H, Woessner Jr JF. Matrix metalloproteinases. J Biol Chem 1999; 274: 21491-4.
    CrossrefPubMedGoogle Scholar
  • 13 Velasco G, Pendas AM, Fueyo A, Knauper V, Murphy G, Lopez-Otin C. Cloning and characterization of human MMP-23, a new matrix metalloproteinase predominantly expressed in reproductive tissues and lacking conserved domains in other family members. J Biol Chem 1999; 274: 4570-6.
    CrossrefPubMedGoogle Scholar
  • 14 Pei D, Weiss SJ. Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 1995; 375: 244-7.
    CrossrefPubMedGoogle Scholar
  • 15 Yang M, Murray MT, Kurkinen A. A novel matrix metalloproteinase gene (XMMP) encoding vitronectin-like motifs is transiently expressed in Xenopus laevis early embryo development. J Biol Chem 1997; 272: 13527-33.
    CrossrefPubMedGoogle Scholar
  • 16 Bode W, Gomis-Ruth FX, Stockler W. Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the ‘metzincins’. FEBS Lett 1993; 331: 134-40.
    CrossrefPubMedGoogle Scholar
  • 17 Allan JA, Docherty AJ, Barker PJ, Huskisson NS, Reynolds JJ, Murphy G. Binding of gelatinases A and B to type-I collagen and other matrix components. Biochem J 1995; 309: 299-306.
    CrossrefPubMedGoogle Scholar
  • 18 Massova I, Kotra LP, Fridman R, Mobashery S. Matrix metalloproteinases: structures, evolution, and diversification. FASEB J 1998; 12: 1075-95.
    CrossrefPubMedGoogle Scholar
  • 19 Murphy G, Willenbrock F, Ward RV, Cockett MI, Eaton D, Docherty AJ. The C-terminal domain of 72 kDa gelatinase A is not required for catalysis, but is essential for membrane activation and modulates interactions with tissue inhibitors of metalloproteinases. Biochem J 1992; 283: 637-41.
    CrossrefPubMedGoogle Scholar
  • 20 Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 1995; 270: 5331-8.
    CrossrefPubMedGoogle Scholar
  • 21 Uria JA, Lopez-Otin C. Matrilysin-2, a new matrix metalloproteinase expressed in human tumors and showing the minimal domain organization required for secretion, latency, and activity. Cancer Res 2000; 60: 4745-51.
    PubMedGoogle Scholar
  • 22 Sato H, Seiki M. Membrane-type matrix metalloproteinases (MT-MMPs) in tumor metastasis. J Biochem (Tokyo) 1996; 119: 209-15.
    CrossrefPubMedGoogle Scholar
  • 23 Nagase H. Activation mechanisms of matrix metalloproteinases. Biol Chem 1997; 378: 151-60.
    PubMedGoogle Scholar
  • 24 Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 2000; 1477: 267-83.
    CrossrefPubMedGoogle Scholar
  • 25 Okada Y, Gonoji Y, Naka K, Tomita K, Nakanishi I, Iwata K, Yamashita K, Hayakawa T. Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT1080 human fibrosarcoma cells. Purification and activation of the precursor and enzymic properties. J Biol Chem 1992; 267: 21712-9.
    PubMedGoogle Scholar
  • 26 Suzuki K, Enghild JJ, Morodomi T, Salvesen G, Nagase H. Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry 1990; 29: 10261-70.
    CrossrefPubMedGoogle Scholar
  • 27 Eeckhout Y, Vaes G. Further studies on the activation of procollagenase, the latent precursor of bone collagenase. Effects of lysosomal cathepsin B, plasmin and kallikrein, and spontaneous activation. Biochem J 1977; 166: 21-31.
    CrossrefPubMedGoogle Scholar
  • 28 He CS, Wilhelm SM, Pentland AP, Marmer BL, Grant GA, Eisen AZ, Goldberg GI. Tissue cooperation in a proteolytic cascade activating human interstitial collagenase. Proc Natl Acad Sci USA 1989; 86: 2632-6.
    CrossrefPubMedGoogle Scholar
  • 29 Baramova EN, Bajou K, Remacle A, L’Hoir C, Krell HW, Weidle UH, Noel A, Foidart JM. Involvement of PA/plasmin system in the processing of proMMP-9 and in the second step of proMMP-2 activation. FEBS Lett 1997; 405: 157-62.
    CrossrefPubMedGoogle Scholar
  • 30 Keski-Oja J, Lohi J, Tuuttila A, Tryggvason K, Vartio T. Proteolytic processing of the 72,000 Da Type IV collagenase by urokinase plasminogen activation. Exp Cell Res 1992; 202: 471-6.
    CrossrefPubMedGoogle Scholar
  • 31 Lijnen HR, Silence J, Van Hoef B, Collen D. Stromelysin-1 (MMP-3)-independent gelatinase expression and activation in mice. Blood 1998; 91: 2045-53.
    PubMedGoogle Scholar
  • 32 Ogata Y, Enghild JJ, Nagase H. Matrix metalloproteinase 3 (stromelysin) activates the precursor of the human matrix metalloproteinase 9. J Biol Chem 1992; 267: 3581-4.
    PubMedGoogle Scholar
  • 33 Ugwu F, Van Hoef B, Bini A, Collen D, Lijnen HR. Proteolytic cleavage of urokinase-type plasminogen activator by stromelysin-1 (MMP-3). Biochemistry 1998; 37: 7231-6.
    CrossrefPubMedGoogle Scholar
  • 34 Marcotte PA, Kozan IM, Dorwin SA, Ryan JM. The matrix metalloproteinase pump-1 catalyzes formation of low molecular weight (pro)urokinase in cultures of normal human kidney cells. J Biol Chem 1992; 267: 13803-6.
    PubMedGoogle Scholar
  • 35 Lijnen HR, Ugwu F, Bini A, Collen D. Generation of an angiostatin-like fragment from plasminogen by stromelysin-1 (MMP-3). Biochemistry 1998; 37: 4699-702.
    CrossrefPubMedGoogle Scholar
  • 36 Patterson BC, Sang QA. Angiostatin-converting enzyme activities of human matrilysin (MMP-7) and gelatinase B/type IV collagenase (MMP-9). J Biol Chem 1997; 272: 28823-5.
    CrossrefPubMedGoogle Scholar
  • 37 Dong Z, Kumar R, Yang X, Fidler IJ. Macrophage-derived metalloelastase is responsible for the generation of angiostatin in Lewis lung carcinoma. Cell 1997; 88: 801-10.
    CrossrefPubMedGoogle Scholar
  • 38 Ugwu F, Lemmens G, Collen D, Lijnen HR. Modulation of cell-associated plasminogen activation by stromelysin-1 (MMP-3). Thromb Haemost 1999; 82: 1127-31.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 39 Bini A, Itoh Y, Kudryk BJ, Nagase H. Degradation of cross-linked fibrin by matrix metalloproteinase 3 (stromelysin 1): hydrolysis of the gamma Gly 404 – Ala 405 peptide bond. Biochemistry 1996; 35: 13056-63.
    CrossrefPubMedGoogle Scholar
  • 40 Bini A, Wu D, Schnuer J, Kudryk BJ. Characterization of stromelysin-1 (MMP-3), matrilysin (MMP-7), and membrane type 1 matrix metalloproteinase (MT1-MMP) derived fibrin(ogen) fragments D-dimer and D-like monomer: NH2-terminal sequences of late-stage digest fragments. Biochemistry 1999; 38: 13928-36.
    CrossrefPubMedGoogle Scholar
  • 41 Lijnen HR, Ugwu F, Rio MC, Collen D. Plasminogen/plasmin and matrix metalloproteinase system function in mice with targeted inactivation of stromelysin-3 (MMP-11). Fibrinolysis & Proteolysis 1998; 12: 155-64.
    CrossrefPubMedGoogle Scholar
  • 42 Rubanyi GM. The role of endothelium in cardiovascular homeostasis and diseases. J Cardiovasc Pharmacol 1993; 22 (Suppl. 04) S1-14.
    CrossrefPubMedGoogle Scholar
  • 43 Ross R. Atherosclerosis – an inflammatory disease. N Engl J Med 1999; 340: 115-26.
    CrossrefPubMedGoogle Scholar
  • 44 Carmeliet P, Collen D. Transgenic mouse models in angiogenesis and cardiovascular disease. J Pathol 2000; 190: 387-405.
    CrossrefPubMedGoogle Scholar
  • 45 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: 2125-31.
    CrossrefPubMedGoogle Scholar
  • 46 Libby P, Geng YJ, Aikawa M, Schoenbeck U, Mach F, Clinton SK, Sukhova GK, Lee RT. Macrophages and atherosclerotic plaque stability. Curr Opin Lipidol 1996; 7: 330-5.
    CrossrefPubMedGoogle Scholar
  • 47 Juhan-Vague I, Collen D. On the role of coagulation and fibrinolysis in atherosclerosis. Ann Epidemiol 1992; 2: 427-38.
    CrossrefPubMedGoogle Scholar
  • 48 Hamsten A, Eriksson P. Fibrinolysis and atherosclerosis: an update. Fibrinolysis 1994; 8: 253-62.
    PubMedGoogle Scholar
  • 49 Schneidermann J, Sawdey MS, Keeton MR, Bordin GM, Bernstein EF, Dilley RB, Loskutoff DJ. Increased type 1 plasminogen activator inhibitor gene expression in atherosclerotic human arteries. Proc Natl Acad Sci USA 1992; 89: 6998-7002.
    CrossrefPubMedGoogle Scholar
  • 50 Newman KM, Jean Claude J, Li H, Scholes JV, Ogata Y, Nagase H, Tilson MD. Cellular localization of matrix metalloproteinase in the abdominal aortic aneurysm wall. J Vasc Surg 1994; 20: 814-20.
    CrossrefPubMedGoogle Scholar
  • 51 Sakalihasan N, Delvenne P, Nusgens BV, Limet R, Lapiere CM. Activated forms of MMP2 and MMP9 in abdominal aortic aneurysms. J Vasc Surg 1996; 24: 127-33.
    CrossrefPubMedGoogle Scholar
  • 52 Schneiderman J, Bordin GM, Engelberg I, Adar R, Seiffert D, Thinnes T, Bernstein EF, Dilley RB, Loskutoff DJ. Expression of fibrinolytic genes in atherosclerotic abdominal aortic aneurysm wall. A possible mechanism for aneurysm expansion. J Clin Invest 1995; 96: 639-45.
    CrossrefPubMedGoogle Scholar
  • 53 Lupu F, Heim DA, Bachmann F, Hurni M, Kakkar VV, Kruithof EK. Plasminogen activator expression in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol 1995; 15: 1444-55.
    CrossrefPubMedGoogle Scholar
  • 54 Galis ZS, Sukhova GK, Kranzhöfer R, Clark S, Libby P. Macrophage foam cells from experimental atheroma constitutively produce matrix-degrading proteinases. Proc Natl Acad Sci USA 1995; 92: 402-6.
    CrossrefPubMedGoogle Scholar
  • 55 Henney AM, Wakely PR, Davies MJ, Foster K, Hembry R, Murphy G, Humphries S. Localization of stromelysin gene expression in atherosclerotic plaques by in situ hybridization. Proc Natl Acad Sci USA 1991; 88: 8154-8.
    CrossrefPubMedGoogle Scholar
  • 56 Galis SZ, Muszynski M, Sukhova GK, Simon-Morrisey E, Libby P. Enhanced expression of vascular matrix metalloproteinases induced in vitro by cytokines and in regions of human atherosclerotic lesions. Ann NY Acad Sci 1995; 748: 501-7.
    PubMedGoogle Scholar
  • 57 Schonbeck J, Mach F, Sukhova GK, Atkinson E, Levesque E, Herman M, Graber P, Basset P, Libby P. Expression of stromelysin-3 in atherosclerotic lesions: regulation via CD40-CD40 ligand signaling in vitro and in vivo. J Exp Med 1999; 189: 843-53.
    CrossrefPubMedGoogle Scholar
  • 58 Rajavashisth TB, Xu XP, Jovinge S, Meisel S, Xu XO, Chai NN, Fischbein MC, Kaul S, Cercek B, Sharifi B, Shah PK. Membrane type 1 matrix metalloproteinase expression in human atherosclerotic plaques: evidence for activation by proinflammatory mediators. Circulation 1999; 99: 3103-9.
    CrossrefPubMedGoogle Scholar
  • 59 Hong BK, Kwon HM, Lee BK, Kim D, Kim IJ, Kang SM, Jang Y, Cho SH, Kim HK, Jang BC, Cho SY, Kim HS, Kim MS, Kwon HC, Lee N. Coexpression of cyclooxygenase-2 and matrix metalloproteinases in human aortic atherosclerotic lesions. Yonsei Med J 2000; 41: 82-8.
    CrossrefPubMedGoogle Scholar
  • 60 Xu XP, Meisel SR, Ong JM, Kaul S, Cercek B, Rajavashisth TB, Sharifi B, Shah PK. Oxidized low-density lipoprotein regulates matrix metalloproteinase-9 and its tissue inhibitor in human monocyte-derived macrophages. Circulation 1999; 99: 993-8.
    CrossrefPubMedGoogle Scholar
  • 61 Moreau M, Brocheriou I, Petit L, Ninio E, Chapman MJ, Rouis M. Inter-leukin-8 mediates downregulation of tissue inhibitor of metalloproteinase-1 expression in cholesterol-loaded human macrophages: relevance to stability of atherosclerotic plaque. Circulation 1999; 99: 420-6.
    CrossrefPubMedGoogle Scholar
  • 62 Fabunmi RP, Sukhova GK, Sugiyama S, Libby P. Expression of tissue inhibitor of metalloproteinases-3 in human atheroma and regulation in lesion-associated cells: a potential protective mechanism in plaque stability. Circ Res 1998; 83: 270-8.
    CrossrefPubMedGoogle Scholar
  • 63 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: 1707-15.
    CrossrefPubMedGoogle Scholar
  • 64 Bocan TM, Krause BR, Rosebury WS, Mueller SB, Lu X, Dagle C, Major T, Lathia C, Lee H. The ACAT inhibitor avasimibe reduces macrophages and matrix metalloproteinase expression in atherosclerotic lesions of hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol 2000; 20: 70-9.
    CrossrefPubMedGoogle Scholar
  • 65 Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 1992; 71: 343-53.
    CrossrefPubMedGoogle Scholar
  • 66 Carmeliet P, Moons L, Lijnen HR, Baes M, Lemaitre V, Tipping P, Drew A, Eeckhout Y, Shapiro S, Lupu F, Collen D. Urokinase-generated plasmin is a candidate activator of matrix metalloproteinases during atherosclerotic aneurysm formation. Nature Genet 1997; 17: 439-44.
    CrossrefPubMedGoogle Scholar
  • 67 Silence J, Collen D, Lijnen HR. Persistance of atherosclerotic plaque and reduced aneurysm formation in mice with stromelysin-1 (MMP-3) gene inactivation. Fibrinolysis & Proteolysis 2000; 14 Suppl 1 12 (Abstract 0-17).
    PubMedGoogle Scholar
  • 68 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: 533-40.
    CrossrefPubMedGoogle Scholar
  • 69 Allaire E, Forough R, Clowes M, Starcher B, Clowes AW. Local overexpression of TIMP-1 prevents aortic aneurysm degeneration and rupture in a rat model. J Clin Invest 1998; 102: 1413-20.
    CrossrefPubMedGoogle Scholar
  • 70 Dollery CM, McEwan JR, Henney AM. Matrix metalloproteinases and cardiovascular disease. Circ Res 1995; 77: 863-8.
    CrossrefPubMedGoogle Scholar
  • 71 Celentano DC, Frishman WH. Matrix metalloproteinases and coronary artery disease: a novel therapeutic target. J Clin Pharmacol 1997; 150: 761-76.
    PubMedGoogle Scholar
  • 72 Galis ZS, Muszynski M, Sukhova GK, Simon-Morrissey E, Unemori EN, Lark MW, Amento E, Libby P. Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion. Circ Res 1994; 75: 181-9.
    CrossrefPubMedGoogle Scholar
  • 73 Halpert I, Sires UI, Roby JD, Potter-Perigo S, Wight TN, Shapiro SD, Welgus HG, Wickline SA, Parks WC. 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 USA 1996; 93: 9748-53.
    CrossrefPubMedGoogle Scholar
  • 74 Irizarry E, Newman KM, Gandhi RH, Nackman GB, Halpern V, Wishner S, Scholes JV, Tilson MD. Demonstration of interstitial collagenase in abdominal aortic aneurysm disease. J Surg Res 1993; 54: 571-4.
    CrossrefPubMedGoogle Scholar
  • 75 Moons L, Shi V, Ploplis V, Plow E, Haber E, Collen D, Carmeliet P. Reduced transplant arteriosclerosis in plasminogen deficient mice. J Clin Invest 1998; 102: 1788-97.
    CrossrefPubMedGoogle Scholar
  • 76 Clowes AW, Clowes MM, Au YP, Reidy MA, Belin D. Smooth muscle cells express urokinase during mitogenesis and tissue-type plasminogen activator during migration in injured rat carotid artery. Circ Res 1990; 67: 61-7.
    CrossrefPubMedGoogle Scholar
  • 77 Jackson CL, Reidy MA. The role of plasminogen activation in smooth muscle cell migration after arterial injury. Ann NY Acad Sci 1992; 667: 141-50.
    CrossrefPubMedGoogle Scholar
  • 78 Reidy MA, Irvin C, Lindner V. Migration of arterial wall cells. Expression of plasminogen activators and inhibitors in injured rat arteries. Circ Res 1996; 78: 405-14.
    CrossrefPubMedGoogle Scholar
  • 79 Bendeck MP, Zempo N, Clowes AW, Galardy RE, Reidy MA. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res 1994; 75: 539-45.
    CrossrefPubMedGoogle Scholar
  • 80 Zempo N, Kenagy RD, Au YPT, Bendeck M, Clowes MM, Reidy MA, Clowes AW. Matrix metalloproteinases of vascular cells are increased in balloon-injured rat carotid artery. J Vasc Surg 1994; 20: 209-17.
    CrossrefPubMedGoogle Scholar
  • 81 Hasenstab D, Forough R, Clowes AW. Plasminogen activator inhibitor type 1 and tissue inhibitor of metalloproteinases-2 increase after arterial injury in rats. Circ Res 1997; 80: 490-6.
    CrossrefPubMedGoogle Scholar
  • 82 Zempo N, Koyama N, Kenagy RD, Lea HJ, Clowes AW. Regulation of vascular smooth muscle cell migration and proliferation in vitro and in injured rat arteries by a synthetic matrix metalloproteinase inhibitor. Arterioscler Thromb Vasc Biol 1996; 16: 28-33.
    CrossrefPubMedGoogle Scholar
  • 83 Forough R, Koyama N, Hasenstab D, Lea H, Clowes M, Nikkari ST, Clowes AW. Overexpression of tissue inhibitor of matrix metalloproteinase-1 inhibits vascular smooth muscle cell functions in vitro and in vivo. Circ Res 1996; 79: 812-20.
    CrossrefPubMedGoogle Scholar
  • 84 George SJ, Johnson JL, Angelini GD, Newby AC, Baker AH. Adenovirus-mediated gene transfer of the human TIMP-1 gene inhibits smooth muscle cell migration and neointimal formation in human saphenous vein. Hum Gene Ther 1998; 9: 867-77.
    CrossrefPubMedGoogle Scholar
  • 85 Kenagy RD, Hart CE, Stetler-Stevenson WG, Clowes AW. Primate smooth muscle cell migration from aortic explants is mediated by endogenous platelet-derived growth factor and basic fibroblast growth factor acting through matrix metalloproteinases 2 and 9. Circulation 1997; 96: 3555-60.
    CrossrefPubMedGoogle Scholar
  • 86 Kenagy RD, Vergel S, Mattsson E, Bendeck M, Reidy MA, Clowes AW. The role of plasminogen, plasminogen activators, and matrix metalloproteinases in primate arterial smooth muscle cell migration. Arterioscler Thromb Vasc Biol 1996; 16: 1373-82.
    CrossrefPubMedGoogle Scholar
  • 87 Aoyagi M, Yamamoto M, Azuma H, Nagashima G, Niimi Y, Tamaki M, Hirakawa K, Yamamoto K. Immunolocalization of matrix metalloproteinases in rabbit carotid arteries after balloon denudation. Histochem Cell Biol 1998; 109: 97-102.
    CrossrefPubMedGoogle Scholar
  • 88 Carmeliet P, Moons L, Ploplis V, Plow E, Collen D. Impaired arterial neointima formation in mice with disruption of the plasminogen gene. J Clin Invest 1997; 99: 200-8.
    CrossrefPubMedGoogle Scholar
  • 89 Carmeliet P, Moons L, Herbert J-M, Crawley J, Lupu F, Lijnen R, Collen D. Urokinase-type but not tissue-type plasminogen activator mediates arterial neointima formation in mice. Circ Res 1997; 81: 829-39.
    CrossrefPubMedGoogle Scholar
  • 90 Shi C, Patel A, Zhang D, Wang H, Carmeliet P, Reed GL, Lee M-E, Haber E, Sibinga NES. Plasminogen is not required for neointima formation in a mouse model of vein graft stenosis. Circ Res 1999; 84: 883-90.
    CrossrefPubMedGoogle Scholar
  • 91 Lijnen HR, Lupu F, Moons L, Carmeliet P, Goulding D, Collen D. Temporal and topographic matrix metalloproteinase expression after vascular injury in mice. Thromb Haemost 1999; 81: 799-807.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 92 Okada A, Tomasetto C, Lutz Y, Bellocq JP, Rio MC, Basset P. Expression of matrix metalloproteinases during rat skin wound healing: evidence that membrane type-1 matrix metalloproteinase is a stromal activator of progelatinase A. J Cell Biol 1997; 137: 67-77.
    CrossrefPubMedGoogle Scholar
  • 93 Shofuda K, Yasumitsu H, Nishihashi A, Miki K, Miyazaki K. Expression of three membrane-type matrix metalloproteinases (MT-MMPs) in rat vascular smooth muscle cells and characterization of MT3-MMPs with and without transmembrane domain. J Biol Chem 1997; 272: 9749-54.
    CrossrefPubMedGoogle Scholar
  • 94 Webb KE, Henney AM, Anglin S, Humphries SE, McEwan JR. Expression of matrix metalloproteinases and their inhibitor TIMP-1 in the rat carotid artery after balloon injury. Arterioscler Thromb Vasc Biol 1997; 17: 1837-44.
    CrossrefPubMedGoogle Scholar
  • 95 Lijnen HR, Van Hoef B, Soloway P, Collen D. Tissue inhibitor type 1 of matrix metalloproteinases (TIMP-1) impairs arterial neointima formation after vascular injury in mice. Circ Res 1999; 85: 1186-91.
    CrossrefPubMedGoogle Scholar
  • 96 Lovdahl C, Thyberg J, Cercek B, Blomgren K, Dimayuga P, Kallin B, Hultgardh-Nilsson A. Antisense oligonucleotides to stromelysin mRNA inhibit injury-induced proliferation of arterial smooth muscle cells. Histol Histopathol 1999; 14: 1101-12.
    PubMedGoogle Scholar
  • 97 Johnson DE, Alderman EL, Schroeder JS, Gao SZ, Hunt S, DeCampli WM, Stinson E, Billingham M. Transplant coronary artery disease: histopathologic correlations with angiographic morphology. J Am Coll Cardiol 1991; 17: 449-57.
    CrossrefPubMedGoogle Scholar
  • 98 Carmeliet P. Proteinases in cardiovascular aneurysms and rupture: targets for therapy?. J Clin Invest 2000; 105: 1519-20.
    CrossrefPubMedGoogle Scholar
  • 99 Thompson RW. Basic science of abdominal aortic aneurysms: emerging therapeutic strategies for an unresolved clinical problem. Curr Opin Cardiol 1996; 11: 504-18.
    CrossrefPubMedGoogle Scholar
  • 100 Dalrymple-Hay MJ, Monro JL, Livesey SA, Lamb RK. Postinfarction ventricular septal rupture: the Wessex experience. Semin Thorac Cardiovasc Surg 1998; 10: 111-6.
    CrossrefPubMedGoogle Scholar
  • 101 Jean Claude J, Newman KM, Li H, Gregory AK, Tilson MD. Possible key role for plasmin in the pathogenesis of abdominal aortic aneurysms. Surgery 1994; 116: 472-8.
    PubMedGoogle Scholar
  • 102 Reilly JM, Sicard GA, Lucore CL. Abnormal expression of plasminogen activators in aortic aneurysmal and occlusive disease. J Vasc Surg 1994; 19: 865-72.
    CrossrefPubMedGoogle Scholar
  • 103 Vine N, Powell JT. Metalloproteinases in degenerative aortic disease. Clin Sci 1991; 81: 233-9.
    CrossrefPubMedGoogle Scholar
  • 104 Newman KM, Ogata Y, Malon AM, Irizarry E, Gandhi RH, Nagase H, Tilson MD. Identification and matrix metalloproteinases 3 (stromelysin-1) and 9 (gelatinase B) in abdominal aortic aneurysm. Arterioscler Thromb 1994; 14: 1315-20.
    CrossrefPubMedGoogle Scholar
  • 105 Thompson RW, Holmes DR, Mertens RA, Liao S, Botney MD, Mecham RP, Welgus HG, Parks WC. Production and localization of 92-kilodalton gelatinase in abdominal aortic aneurysms: an elastolytic metalloproteinase expressed by aneurysm-infiltrating macrophages. J Clin Invest 1995; 96: 318-26.
    CrossrefPubMedGoogle Scholar
  • 106 McMillan WD, Patterson BK, Keen RR, Shively VP, Cipollone M, Pearce WH. In situ localization and quantification of mRNA for 92-kD type IV collagenase and its inhibitor in aneurysmal, occlusive, and normal aorta. Arterioscler Thromb Vasc Biol 1995; 15: 1139-44.
    CrossrefPubMedGoogle Scholar
  • 107 Newman KM, Jean Claude J, Li H, Scholes JV, Ogata Y, Nagase H. Cellular localization of matrix metalloproteinases in the abdominal aortic aneurysm wall. J Vasc Surg 1994; 20: 814-20.
    CrossrefPubMedGoogle Scholar
  • 108 Curci JA, Liao S, Huffman MD, Shapiro SD, Thompson RW. Expression and localization of macrophage elastase (matrix metalloproteinase-12) in abdominal aortic aneurysms. J Clin Invest 1998; 102: 1900-10.
    CrossrefPubMedGoogle Scholar
  • 109 Allaire E, Hasenstab D, Kenagy RD, Starcher B, Clowes MM, Clowes AW. Prevention of aneurysm development and rupture by local overexpression of plasminogen activator inhibitor-1. Circulation 1998; 98: 249-55.
    CrossrefPubMedGoogle Scholar
  • 110 Thompson RW, Baxter BT. MMP inhibition in abdominal aortic aneurysms. Rationale for a prospective randomized clinical trial. Annals NY Acad Sci 1999; 878: 159-78.
    CrossrefPubMedGoogle Scholar
  • 111 Pyo R, Lee JK, Shipley JM, Curci JA, Mao D, Ziporin SJ, Ennis TL, Shapiro SD, Senior RM, Thompson RW. Targeted gene disruption of matrix metalloproteinase-9 (gelatinase B) suppresses development of experimental abdominal aortic aneurysms. J Clin Invest 2000; 105: 1641-9.
    CrossrefPubMedGoogle Scholar
  • 112 Heymans S, Luttun A, Nuyens D, Theilmeier G, Creemers E, Moons L, Dyspersin GD, Cleutjens JPM, Shipley M, Angellillo A, Levi M, Nübe O, Baker A, Keshet E, Lupu F, Herbert J-M, Smiths FJM, Shapiro SD, Baes M, Borgers M, Collen D, Daemen MJAP, Carmeliet P. Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure. Nature Med 1999; 5: 1135-42.
    CrossrefPubMedGoogle Scholar
  • 113 Reddy SG, Roberts W. C. Frequency of rupture of the left ventricular free wall or ventricular septum among necropsy cases of fatal acute myocardial infarction since introduction of coronary care units. Am J Cardiol 1989; 63: 906-11.
    CrossrefPubMedGoogle Scholar
  • 114 Varbella F, Bongioanni S, Sibona-Masi A, Iazzolino E, Alunni G, Conte MR, Brusca A. Subacute left ventricular free-wall rupture in early course of acute myocardial infarction. Clinical report of two cases and review of the literature. G Ital Cardiol 1999; 29: 163-70.
    PubMedGoogle Scholar
  • 115 Knoepfler PS, Bloor CM, Carroll SM. Urokinase plasminogen activator activity is increased in the myocardium during coronary artery occlusion. J Mol Cell Cardiol 1995; 27: 1317-24.
    CrossrefPubMedGoogle Scholar
  • 116 Rohde LE, Ducharme A, Arroyo LH, Aikawa M, Sukhova GH, Lopez-Anaya A, McClure KF, Mitchell PG, Libby P, Lee RT. Matrix metalloproteinase inhibition attenuates early left ventricular enlargement after experimental myocardial infarction in mice. Circulation 1999; 99: 3063-70.
    CrossrefPubMedGoogle Scholar
  • 117 Cleutjens JPM, Kandala JC, Guarda E, Guntaka RV, Weber KT. Regulation of collagen degradation in the rat myocardium after infarction. J Mol Cell Cardiol 1995; 27: 1281-92.
    CrossrefPubMedGoogle Scholar
  • 118 Thomas CV, Coker ML, Zellner JL, Handy JR, Crumbley AJ III, Spinale FG. Increased matrix metalloproteinase activity and selective upregulation in LV myocardium from patients with end-stage dilated cardiomyopathy. Circulation 1998; 97: 1708-15.
    CrossrefPubMedGoogle Scholar
  • 119 Coker ML, Thomas CV, Clair MJ, Hendrick JW, Kombrach RS, Galis ZS, Spinale FG. Myocardial matrix metalloproteinase activity and abundance with congestive heart failure. Am J Physiol 1998; 274: H1516-23.
    PubMedGoogle Scholar
  • 120 Robert V, Besse S, Sabri A, Silvestre JS, Assayag P, Nguyen VT, Swynghedauw B, Delcayre C. Differential regulation of matrix metalloproteinases associated with aging and hypertension in the rat heart. Lab Invest 1997; 76: 729-38.
    PubMedGoogle Scholar
  • 121 Tyagi SC, Kumar S, Cassatt S, Parker JL. Temporal expression of extracellular matrix metalloproteinases and tissue plasminogen activator in the development of collateral vessels in the canine model of coronary occlusion. Can J Physiol Pharmacol 1996; 74: 983-995.
    PubMedGoogle Scholar
  • 122 Spinale FG, Krombach RS, Coker ML, Mukherjee R, Houck WV, Clair MJ, Kribbs SB, Hebbar L, Peterson JT. Matrix metalloproteinase inhibition with congestive heart failure improves left ventricular geometry and pump function. Circulation. 1997 96. Suppl. I I-520 (Abstract).
    PubMedGoogle Scholar
  • 123 Peterson JT, Rosebury WS, Robertson AW, Washington RA, Li H, O’Brien PM, Sliskovic DR, Hallak H, Uprichard ACG, Bocan TMA. Matrix metalloproteinase inhibition blocks progression of heart failure. Circulation. 1997 96. Suppl. I I-520 (Abstract).
    PubMedGoogle Scholar