Platelets and matrix metalloproteinases

Peter Seizer; Andreas E. May

doi:10.1160/TH13-02-0113

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2013; 110(05): 903-909
DOI: 10.1160/TH13-02-0113

Theme Issue Article

Schattauer GmbH

Platelets and matrix metalloproteinases

Autoren

Peter Seizer

¹Medizinische Klinik III, Eberhard Karls Universität Tübingen, Germany
Andreas E. May

¹Medizinische Klinik III, Eberhard Karls Universität Tübingen, Germany

Abstract

Summary

Matrix metalloproteinases (MMPs) and their inhibitors essentially contribute to a variety of pathophysiologies by modulating cell migration, tissue degradation and inflammation. Platelet-associated MMP activity appears to play a major role in these processes. First, platelets can concentrate leukocyte-derived MMP activity to sites of vascular injury by leukocyte recruitment. Second, platelets stimulate MMP production in e.g. leukocytes, endothelial cells, or tumour cells by direct receptor interaction or/and by paracrine pathways. Third, platelets synthesise and secrete a variety of MMPs including MMP-1, MMP-2, MMP-3, and MMP-14 (MT1-MMP), and potentially MMP-9 as well as the tissue inhibitors of metalloproteinase (TIMPs). This review focuses on platelet-derived and platelet-induced MMPs and their inhibitors.

Keywords

Platelets - MMP - EMMPRIN

Volltext

Referenzen

References
1 Liu P, Sun M, Sader S. Matrix metalloproteinases in cardiovascular disease. Can J Cardiol 2006; 22 B 25B-30B.
2 Berry E, Bosonea AM, Wang X. et al. Insights into the activity, differential expression, mutual regulation, and functions of matrix metalloproteinases and a disintegrin and metalloproteinases in hypertension and cardiac disease. J Vasc Res 2013; 50: 52-68.
3 Folgueras AR, Pendas AM, Sanchez LM. et al. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol 2004; 48: 411-424.
4 Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 2002; 115: 3719-3727.
5 Brew K, Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta 2010; 1803: 55-71.
6 Gross J, Lapiere CM. Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci USA 1962; 48: 1014-1022.
7 Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007; 8: 221-233.
8 Chen WT, Wang JY. Specialized surface protrusions of invasive cells, invadopodia and lamellipodia, have differential MT1-MMP, MMP-2, and TIMP-2 localisation. Ann NY Acad Sci 1999; 878: 361-371.
9 Estreicher A, Muhlhauser J, Carpentier JL. et al. The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. J Cell Biol 1990; 111: 783-792.
10 Brown PD, Bloxidge RE, Stuart NS. et al. Association between expression of activated 72-kilodalton gelatinase and tumour spread in non-small-cell lung carcinoma. J Natl Cancer Inst 1993; 85: 574-578.
11 Azzam HS, Arand G, Lippman ME. et al. Association of MMP-2 activation potential with metastatic progression in human breast cancer cell lines independent of MMP-2 production. J Natl Cancer Inst 1993; 85: 1758-1764.
12 Seizer P, Klingel K, Sauter M. et al. Cyclophilin A affects inflammation, virus elimination and myocardial fibrosis in coxsackievirus B3-induced myocarditis. J Mol Cell Cardiol 2012; 53: 6-14.
13 Cheung C, Marchant D, Walker EK. et al. Ablation of matrix metalloproteinase-9 increases severity of viral myocarditis in mice. Circulation 2008; 117: 1574-1582.
14 Seizer P, Geisler T, Bigalke B. et al. EMMPRIN and its ligand Cyclophilin A as novel diagnostic markers in inflammatory cardiomyopathy. Int J Cardiol 2013; 163: 299-304.
15 Rahman M, Roller J, Zhang S. et al. Metalloproteinases regulate CD40L shedding from platelets and pulmonary recruitment of neutrophils in abdominal sepsis. Inflamm Res 2012; 61: 571-579.
16 Westermann D, Savvatis K, Lindner D. et al. Reduced degradation of the chemokine MCP-3 by matrix metalloproteinase-2 exacerbates myocardial inflammation in experimental viral cardiomyopathy. Circulation 2011; 124: 2082-2093.
17 Heissig B, Hattori K, Dias S. et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002; 109: 625-637.
18 May AE, Kalsch T, Massberg S. et al. Engagement of glycoprotein IIb/IIIa (alpha (IIb)beta3) on platelets upregulates CD40L and triggers CD40L-dependent matrix degradation by endothelial cells. Circulation 2002; 106: 2111-2117.
19 Weber C. Platelets and chemokines in atherosclerosis: partners in crime. Circ Res 2005; 96: 612-616.
20 Galt SW, Lindemann S, Medd D. et al. Differential regulation of matrix metalloproteinase-9 by monocytes adherent to collagen and platelets. Circ Res 2001; 89: 509-516.
21 May AE, Seizer P, Gawaz M. Platelets: inflammatory firebugs of vascular walls. Arterioscler Thromb Vasc Biol 2008; 28: s5-10.
22 Janowska-Wieczorek A, Wysoczynski M, Kijowski J. et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 2005; 113: 752-760.
23 Seizer P, Gawaz M, May AE. Platelet-monocyte interactions--a dangerous liaison linking thrombosis, inflammation and atherosclerosis. Curr Med Chem 2008; 15: 1976-1980.
24 Sawicki G, Salas E, Murat J. et al. Release of gelatinase A during platelet activation mediates aggregation. Nature 1997; 386: 616-619.
25 Galt SW, Lindemann S, Allen L. et al. Outside-in signals delivered by matrix metalloproteinase-1 regulate platelet function. Circ Res 2002; 90: 1093-1099.
26 Kazes I, Elalamy I, Sraer JD. et al. Platelet release of trimolecular complex components MT1-MMP/TIMP2/MMP2: involvement in MMP2 activation and platelet aggregation. Blood 2000; 96: 3064-3069.
27 Cecchetti L, Tolley ND, Michetti N. et al. Megakaryocytes differentially sort mRNAs for matrix metalloproteinases and their inhibitors into platelets: a mechanism for regulating synthetic events. Blood 2011; 118: 1903-1911.
28 Chesney CM, Harper E, Colman RW. Human platelet collagenase. J Clin Invest 1974; 53: 1647-1654.
29 Trivedi V, Boire A, Tchernychev B. et al. Platelet matrix metalloprotease-1 mediates thrombogenesis by activating PAR1 at a cryptic ligand site. Cell 2009; 137: 332-343.
30 Austin KM, Covic L, Kuliopulos A. Matrix metalloproteases and PAR1 activation. Blood 2013; 121: 431-439.
31 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: 1070-1076.
32 Suzuki H, Kusuyama T, Sato R. et al. Elevation of matrix metalloproteinases and interleukin-6 in the culprit coronary artery of myocardial infarction. Eur J Clin Invest 2008; 38: 166-173.
33 Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 2002; 90: 251-262.
34 Sawicki G, Sanders EJ, Salas E. et al. Localisation and translocation of MMP-2 during aggregation of human platelets. Thromb Haemost 1998; 80: 836-839.
35 Falcinelli E, Guglielmini G, Torti M. et al. Intraplatelet signalling mechanisms of the priming effect of matrix metalloproteinase-2 on platelet aggregation. J Thromb Haemost 2005; 3: 2526-2535.
36 Santos-Martinez MJ, Medina C, Jurasz P. et al. Role of metalloproteinases in platelet function. Thromb Res 2008; 121: 535-542.
37 Choi WS, Jeon OH, Kim HH. et al. MMP-2 regulates human platelet activation by interacting with integrin alphaIIbbeta3. J Thromb Haemost 2008; 6: 517-523.
38 Choi WS, Jeon OH, Kim DS. CD40 ligand shedding is regulated by interaction between matrix metalloproteinase-2 and platelet integrin alpha (IIb)beta (3). J Thromb Haemost 2010; 8: 1364-1371.
39 Schonbeck U, Mach F, Sukhova GK. et al. Regulation of matrix metalloproteinase expression in human vascular smooth muscle cells by T lymphocytes: a role for CD40 signalling in plaque rupture?. Circ Res 1997; 81: 448-454.
40 Mach F, Schonbeck U, Fabunmi RP. et al. T lymphocytes induce endothelial cell matrix metalloproteinase expression by a CD40L-dependent mechanism: implications for tubule formation. Am J Pathol 1999; 154: 229-238.
41 Momi S, Falcinelli E, Giannini S. et al. Loss of matrix metalloproteinase 2 in platelets reduces arterial thrombosis in vivo. J Exp Med 2009; 206: 2365-2379.
42 Gresele P, Falcinelli E, Loffredo F. et al. Platelets release matrix metalloproteinase-2 in the coronary circulation of patients with acute coronary syndromes: possible role in sustained platelet activation. Eur Heart J 2011; 32: 316-325.
43 Volcik KA, Campbell S, Chambless LE. et al. MMP2 genetic variation is associated with measures of fibrous cap thickness: The Atherosclerosis Risk in Communities Carotid MRI Study. Atherosclerosis 2010; 210: 188-193.
44 Falcinelli E, Giannini S, Boschetti E. et al. Platelets release active matrix metalloproteinase-2 in vivo in humans at a site of vascular injury: lack of inhibition by aspirin. Br J Haematol 2007; 138: 221-230.
45 Kalvegren H, Jonsson S, Jonasson L. Release of matrix metalloproteinases-1 and -2, but not -9, from activated platelets measured by enzyme-linked immunosorbent assay. Platelets 2011; 22: 572-578.
46 Wrzyszcz A, Wozniak M. On the origin of matrix metalloproteinase-2 and -9 in blood platelets. Platelets 2012; 23: 467-474.
47 Galvez BG, Matias-Roman S, Albar JP. et al. Membrane type 1-matrix metalloproteinase is activated during migration of human endothelial cells and modulates endothelial motility and matrix remodeling. J Biol Chem 2001; 276: 37491-37500.
48 Seiki M. Membrane-type matrix metalloproteinases. APMIS 1999; 107: 137-143.
49 Radomski A, Jurasz P, Sanders EJ. et al. Identification, regulation and role of tissue inhibitor of metalloproteinases-4 (TIMP-4) in human platelets. Br J Pharmacol 2002; 137: 1330-1338.
50 Satoh K, Nigro P, Matoba T. et al. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med 2009; 15: 649-656.
51 Nigro P, Satoh K, O’Dell MR. et al. Cyclophilin A is an inflammatory mediator that promotes atherosclerosis in apolipoprotein E-deficient mice. J Exp Med 2011; 208: 53-66.
52 Romanic AM, Harrison SM, Bao W. et al. Myocardial protection from ischaemia/reperfusion injury by targeted deletion of matrix metalloproteinase-9. Cardiovasc Res 2002; 54: 549-558.
53 Ducharme A, Frantz S, Aikawa M. et al. Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest 2000; 106: 55-62.
54 Matsumura S, Iwanaga S, Mochizuki S. et al. Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice. J Clin Invest 2005; 115: 599-609.
55 Johnson JL, Baker AH, Oka K. et al. Suppression of atherosclerotic plaque progression and instability by tissue inhibitor of metalloproteinase-2: involvement of macrophage migration and apoptosis. Circulation 2006; 113: 2435-2444.
56 Moreno PR, Falk E, Palacios IF. et al. Macrophage infiltration in acute coronary syndromes. Implications for plaque rupture. Circulation 1994; 90: 775-778.
57 Newby AC. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 2005; 85: 1-31.
58 Frangogiannis NG, Smith CW, Entman ML. The inflammatory response in myocardial infarction. Cardiovasc Res 2002; 53: 31-47.
59 Schmidt R, Bultmann A, Fischel S. et al. Extracellular matrix metalloproteinase inducer (CD147) is a novel receptor on platelets, activates platelets, and augments nuclear factor kappaB-dependent inflammation in monocytes. Circ Res 2008; 102: 302-309.
60 Pennings GJ, Yong AS, Kritharides L. Expression of EMMPRIN (CD147) on circulating platelets in vivo. J Thromb Haemost 2010; 8: 472-481.
61 Seizer P, Borst O, Langer HF. et al. EMMPRIN (CD147) is a novel receptor for platelet GPVI and mediates platelet rolling via GPVI-EMMPRIN interaction. Thromb Haemost 2009; 101: 682-686.
62 Schulz C, von Bruhl ML, Barocke V. et al. EMMPRIN (CD147/basigin) mediates platelet-monocyte interactions in vivo and augments monocyte recruitment to the vascular wall. J Thromb Haemost 2011; 9: 1007-1019.
63 Fischer G, Bang H, Mech C. Determination of enzymatic catalysis for the cis-trans-isomerisation of peptide binding in proline-containing peptides. Biomed Biochim Acta 1984; 43: 1101-1111.
64 Seizer P, Schonberger T, Schott M. et al. EMMPRIN and its ligand cyclophilin A regulate MT1-MMP, MMP-9 and M-CSF during foam cell formation. Atherosclerosis 2010; 209: 51-57.
65 Hibino T, Sakaguchi M, Miyamoto S. et al. S100A9 is a novel ligand of EMMPRIN that promotes melanoma metastasis. Cancer Res 2013; 73: 172-183.
66 Weyrich AS, Denis MM, Kuhlmann-Eyre JR. et al. Dipyridamole selectively inhibits inflammatory gene expression in platelet-monocyte aggregates. Circulation 2005; 111: 633-642.
67 Dixon DA, Tolley ND, Bemis-Standoli K. et al. Expression of COX-2 in platelet-monocyte interactions occurs via combinatorial regulation involving adhesion and cytokine signalling. J Clin Invest 2006; 116: 2727-2738.
68 Abou-Saleh H, Theoret JF, Yacoub D. et al. Neutrophil P-selectin-glycoprotein-ligand-1 binding to platelet P-selectin enhances metalloproteinase 2 secretion and platelet-neutrophil aggregation. Thromb Haemost 2005; 94: 1230-1235.
69 Wize J, Sopata I, Smerdel A. et al. Ligation of selectin L and integrin CD11b/CD18 (Mac-1) induces release of gelatinase B (MMP-9) from human neutrophils. Inflamm Res 1998; 47: 325-327.
70 Liu O, Jia L, Liu X. et al. Clopidogrel, a Platelet P2Y12 Receptor Inhibitor, Reduces Vascular Inflammation and Angiotensin II Induced-Abdominal Aortic Aneurysm Progression. PLoS One 2012; 7: e51707
71 Liu Y, Gao XM, Fang L. et al. Novel role of platelets in mediating inflammatory responses and ventricular rupture or remodeling following myocardial infarction. Arterioscler Thromb Vasc Biol 2011; 31: 834-841.
72 Kraemer BF, Borst O, Gehring EM. et al. PI3 kinase-dependent stimulation of platelet migration by stromal cell-derived factor 1 (SDF-1). J Mol Med 2010; 88: 1277-1288.
73 Stach K, Nguyen XD, Lang S. et al. Simvastatin and atorvastatin attenuate VCAM-1 and uPAR expression on human endothelial cells and platelet surface expression of CD40 ligand. Cardiol J 2012; 19: 20-28.
74 Fernandez B I, Alvarez MT, Lopez-Longo FJ. et al. Platelet soluble CD40L and matrix metalloproteinase 9 activity are proinflammatory mediators in Behcet disease patients. Thromb Haemost 2012; 107: 88-98.
75 Menchen L, Marin-Jimenez I, Rias-Salgado EG. et al. Matrix metalloproteinase 9 is involved in Crohn’s disease-associated platelet hyperactivation through the release of soluble CD40 ligand. Gut 2009; 58: 920-928.
76 Karpatkin S, Pearlstein E, Ambrogio C. et al. Role of adhesive proteins in platelet tumour interaction in vitro and metastasis formation in vivo. J Clin Invest 1988; 81: 1012-1019.
77 Erpenbeck L, Schon MP. Deadly allies: the fatal interplay between platelets and metastasising cancer cells. Blood 2010; 115: 3427-3436.
78 Alonso-Escolano D, Strongin AY, Chung AW. et al. Membrane type-1 matrix metalloproteinase stimulates tumour cell-induced platelet aggregation: role of receptor glycoproteins. Br J Pharmacol 2004; 141: 241-252.
79 Lonsdorf AS, Kramer BF, Fahrleitner M. et al. Engagement of alphaIIbbeta3 (GPIIb/IIIa) with alphanubeta3 integrin mediates interaction of melanoma cells with platelets: a connection to hematogenous metastasis. J Biol Chem 2012; 287: 2168-2178.
80 Bourboulia D, Stetler-Stevenson WG. Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): Positive and negative regulators in tumour cell adhesion. Semin Cancer Biol 2010; 20: 161-168.
81 Pearlstein E, Salk PL, Yogeeswaran G. et al. Correlation between spontaneous metastatic potential, platelet-aggregating activity of cell surface extracts, and cell surface sialylation in 10 metastatic-variant derivatives of a rat renal sarcoma cell line. Proc Natl Acad Sci USA 1980; 77: 4336-4339.
82 Belloc C, Lu H, Soria C. et al. The effect of platelets on invasiveness and protease production of human mammary tumour cells. Int J Cancer 1995; 60: 413-417.
83 Jurasz P, Onso-Escolano D, Radomski MW. Platelet--cancer interactions: mechanisms and pharmacology of tumour cell-induced platelet aggregation. Br J Pharmacol 2004; 143: 819-826.
84 Nierodzik ML, Plotkin A, Kajumo F. et al. Thrombin stimulates tumour-platelet adhesion in vitro and metastasis in vivo. J Clin Invest 1991; 87: 229-236.
85 Suzuki K, Aiura K, Ueda M. et al. The influence of platelets on the promotion of invasion by tumour cells and inhibition by antiplatelet agents. Pancreas 2004; 29: 132-140.
86 Onso-Escolano D, Medina C, Cieslik K. et al. Protein kinase C delta mediates platelet-induced breast cancer cell invasion. J Pharmacol Exp Ther 2006; 318: 373-380.
87 Medina C, Jurasz P, Santos-Martinez MJ. et al. Platelet aggregation-induced by caco-2 cells: regulation by matrix metalloproteinase-2 and adenosine diphosphate. J Pharmacol Exp Ther 2006; 317: 739-745.
88 Chung AW, Radomski A, Onso-Escolano D. et al. Platelet-leukocyte aggregation induced by PAR agonists: regulation by nitric oxide and matrix metalloproteinases. Br J Pharmacol 2004; 143: 845-855.
89 Hudson MP, Armstrong PW, Ruzyllo W. et al. Effects of selective matrix metalloproteinase inhibitor (PG-116800) to prevent ventricular remodeling after myocardial infarction: results of the PREMIER (Prevention of Myocardial Infarction Early Remodeling) trial. J Am Coll Cardiol 2006; 48: 15-20.
90 Franco C, Ho B, Mulholland D. et al. Doxycycline alters vascular smooth muscle cell adhesion, migration, and reorganisation of fibrillar collagen matrices. Am J Pathol 2006; 168: 1697-1709.
91 Dalvi PS, Singh A, Trivedi HR. et al. Effect of doxycycline in patients of moderate to severe chronic obstructive pulmonary disease with stable symptoms. Ann Thorac Med 2011; 6: 221-226.