The effect of plasminogen activator inhibitor type 1 on apoptosis

David J. Schneider; Yabing Chen; Burton E. Sobel

doi:10.1160/TH08-04-0234

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2008; 100(06): 1037-1040
DOI: 10.1160/TH08-04-0234

Theme Issue Article

Schattauer GmbH

The effect of plasminogen activator inhibitor type 1 on apoptosis

David J. Schneider

¹Department of Medicine and the Cardiovascular Research Institute, University of Vermont, Burlington, Vermont, USA

,

Yabing Chen

²Department of Pathology, University of Alabama at Birmingham, Birmingham, Alabama, USA

,

Burton E. Sobel

¹Department of Medicine and the Cardiovascular Research Institute, University of Vermont, Burlington, Vermont, USA

› Author Affiliations

Abstract

Summary

Plasminogen activator inhibitor type-1 (PAI-1), an inhibitor of plasminogen activators, inhibits formation of plasmin and plasmin-mediated proteolysis. Apoptosis,or programmed cell death, is a potentially important phenomenon in mediating overall cell death. This review focuses on the influence of PAI-1 on apoptosis. Greater expression of PAI-1 has been associated with increased survival of cells and resistance to apoptosis. PAI-1 appears to influence apoptosis by decreasing cell adhesion (anoikis) as well as its effect on intracellular signaling. Mechanisms by which PAI-1 may render a cell resistant to apoptosis include its ability to inhibit generation of plasmin,its ability to inhibit caspase 3, and its ability to inhibit cell adhesion mediated by vitronectin. Inhibition of caspase 3 by PAI-1 may divert intracellular signalling from induction of apoptosis to induction of proliferation.

Keywords

Plasminogen activator inhibitor - apoptosis - vascular remodelling - cancer

Full Text

References

References
1 Dellas C, Loskutoff DJ. Historical analysis of PA I-1 from its discovery to its potential role in cell motility and disease. Thromb Haemost 2005; 93: 631-640.
2 Czekay RP, Aertgeerts K, Curriden SA. et al. Plas minogen activator inhibitor-1 detaches cells from extracellular matrices by inactivating integrins. J Cell Biol 2003; 160: 781-791.
3 Meilhac O, Ho-Tin-Noe B, Houard X. et al. Pericel lular plasmin induces smooth muscle cell anoikis. Faseb J 2003; 17: 1301-1303.
4 Pandolfi A, Cetrullo D, Polishuck R. et al. Plas minogen activator inhibitor type 1 is increased in the arterial wall of type II diabetic subjects. Arterioscler Thromb Vasc Biol 2001; 21: 1378-1382.
5 Sobel BE, Woodcock-Mitchell J, Schneider DJ. et al. Increased plasminogen activator inhibitor type 1 in coronary artery atherectomy specimens from type 2 diabetic compared with nondiabetic patients:a potential factor predisposing to thrombosis and its persistence. Circulation 1998; 97: 2213-2221.
6 Stone KE, Chiquette E, Chilton RJ. Diabetic endov ascular disease: role of coronary artery revasculariz ation. Am J Cardiol 2007; 99: 105B-112B.
7 De Young MB, Tom C, Dichek DA. Plasminogen activator inhibitor type 1 increases neointima formation in balloon-injured rat carotid arteries. Circulation 2001; 104: 1972-1971.
8 Peng L, Bhatia N, Parker AC. et al. Endogenous vitronectin and plasminogen activator inhibitor-1 promote neointima formation in murine carotid arteries. Arterioscler Thromb Vasc Biol 2002; 22: 934-939.
9 Schneider DJ, Hayes M, Wadsworth M. et al. Attenuation of neointimal vascular smooth muscle cellularity in atheroma by plasminogen activator inhibitor type-1 (PAI-1). J Histochem Cytochem 2004; 52: 1091-1099.
10 Sobel BE. The potential influence of insulin and plasminogen activator inhibitor ty-e-1 on formulation of vulnerable atherosclerotic plaques associated with type 2 diabetes. Proc Assoc Am Phys 1999; 111: 313-318.
11 Noda-Heiny H, Sobel BE. Vascular smooth muscle cell migration mediated by thrombin and urokinasetype plasminogen activator receptor. Am J Physiol 1995; 268: C1195-C1201.
12 Ploplis VA, Castellino FJ. Attenuation of neointima formation following arterial injury in PA I-1 deficient mice. Ann NY Acad Sci 2001; 936: 466-468.
13 Rossignol P, Luttun A, Martin-Ventura JL. et al. Plasminogen activation: a mediator of vascular smooth muscle cell apoptosis in atherosclerotic plaques. J Thromb Haemost 2006; 04: 664-670.
14 Xiang G, Schuster MD, Seki T, Witkowski P, Eshghi S, Itescu S. Downregulated expression of plasminogen activator inhibitor-1 augments myocardial neovascularization and reduces cardiomyocyte apoptosis after acute myocardial infarction. J Am Coll Cardiol 2005; 46: 536-541.
15 Zaman AKMT, Fujii S, Schneider DJ. et al. Deleterious Effects of Lack of Cardiac PAI-1 after Coronary Occlusion in Mice and Their Pathophysiologic Determinants. J Histochem Cytochem 2007; 128: 135-145.
16 Taatjes DJ, Wadsworth MP, Zaman AK. et al. A novel dual staining method for identification of apoptotic cells reveals a modest apoptotic response in infarcted mouse myocardium. Histochem Cell Biol 2007; 128: 275-283.
17 Spurgers KB, Chari NS, Bohnenstiel NL. et al. Molecular mediators of cell death in multistep carcinogenesis: a path to targeted therapy. Cell Death Diff 2006; 13: 1360-1370.
18 Andreasen PA, Kjøller L, Christensen L. et al. The urokinase-type plasminogen activator system in cancer metastasis: a review. Int J Cancer 1997; 72: 1-22.
19 Zhao H, Morimoto T, Sasa M. et al. Immunohistochemical expression of uPA, PAI-1, cathepsin D and apoptotic cells in ductal carcinoma in situ of the breast. Breast Cancer 2002; 09: 118-126.
20 Sugiura Y, Ma L, Sun B. et al. The plasminogenplasminogen activator (PA) system in neuroblastoma: role of PA inhibitor-1 in metastasis. Cancer Res 1999; 59: 1327-1336.
21 Gutierrez LS, Schulman A, Brito-Robinson T. et al. Tumor development is retarded in mice lacking the gene for urokinase-type plasminogen activator or its inhibitor, plasminogen activator inhibitor-1. Cancer Res 2000; 60: 5839-5847.
22 Kwaan HC, Wang J, Svoboda K. et al. Plasminogen activator inhibitor 1 may promote tumour growth through inhibition of apoptosis. Br J Cancer 2000; 82: 1702-1708.
23 Rossignol P, Ho-Tin-Noé B, Vranckx R. et al. Protease nexin-1 inhibits plasminogen activation-induced apoptosis of adherent cells. J Biol Chem 2004; 279: 10346-10356.
24 Rømer MU, Kirkebjerg Due A, Knud Larsen J. et al. Indication of a role of plasminogen activator inhibitor type I in protecting murine fibrosarcoma cells against apoptosis. Thromb Haemost 2005; 94: 859-866.
25 Lademann U, Rømer MU, Jensen PB. et al. Malignant transformation of wild-type but not plasminogen activator inhibitor-1 gene-deficient fibroblasts decreases cellular sensitivity to chemotherapy-mediated apoptosis. Eur J Cancer 2005; 41: 1095-1100.
26 Zoellner H, Höfler M, Beckmann R. et al. Fibrinolytic proteins in apoptotic human umbilical vein endothelial cells. Thromb Res 1998; 91: 209-219.
27 Chen Y, Kelm RJ, Budd RC. et al. Inhibition of apoptosis and caspase-3 in vascular smooth muscle cells by plasminogen activator inhibitor type-1. J Cell Biochem 2004; 92: 178-188.
28 Soeda S, Oda M, Ochiai T. et al. Deficient release of plasminogen activator inhibitor-1 from astrocytes triggers apoptosis in neuronal cells. Brain Res Mol Brain Res 2001; 91: 96-103.
29 Rossignol P, Anglès-Cano E, Lijnen HR. Plasminogen activator inhibitor-1 impairs plasminogen activation-mediated vascular smooth muscle cell apoptosis. Thromb Haemost 2006; 96: 665-670.
30 Horowitz JC, Rogers DS, Simon RH. et al. Plasminogen activation induced pericellular fibronectin proteolysis promotes fibroblast apoptosis. Am J Respir Cell Mol Biol 2008; 38: 78-87.
31 Mali RS, Cheng M, Chintala SK. Plasminogen activators promote excitotoxicity-induced retinal damage. FASEB J 2005; 19: 1280-1289.
32 Reijerkerk A, Mosnier LO, Kranenburg O. et al. Amyloid endostatin induces endothelial cell detachment by stimulation of the plasminogen activation system. Mol Cancer Res 2003; 01: 561-568.
33 Tonner E, Allan G, Shkreta L. et al. Insulin-like growth factor binding protein-5 (IGFBP-5) potentially regulates programmed cell death and plasminogen activation in the mammarygland. Adv Exp Med Biol 2000; 480: 45-53.
34 Flavin MP, Zhao G, Ho LT. Microglial tissue plasminogen activator (tPA) triggers neuronal apoptosis in vitro. Glia 2000; 29: 347-354.
35 Davis J, Wagner MR, Zhang W. et al. Amyloid beta protein stimulates the expression of urokinase-type plasminogen activator (uPA) and its receptor (uPAR) in human cerebrovascular smooth muscle cells. J Biol Chem 2003; 278: 19054-19061.
36 Zhang X, Chaudhry A, Chintala SK. Inhibition of plasminogen activation protects against ganglion cell loss in a mouse model of retinal damage. Mol Vis 2003; 09: 238-248.
37 Lindstedt KA, Leskinen MJ, Kovanen PT. Proteolysis of the pericellular matrix: a novel element determining cell survival and death in the pathogenesis of plaque erosion and rupture. Arterioscler Thromb Vasc Biol 2004; 24: 1350-1358.
38 Al-Fakhri N, Chavakis T, Schmidt-Wöll T. et al. Induction of apoptosis in vascular cells by plasminogen activator inhibitor-1 and high molecular weight kininogen correlates with their antiadhesive properties. Biol Chem 2003; 384: 423-435.
39 Balsara RD, Castellino FJ, Ploplis VA. A novel function of plasminogen activator inhibitor-1 in modulation of the AKT pathway in wild-type and plasminogen activator inhibitor-1-deficient endothelial cells. J Biol Chem 2006; 281: 22527-22536.
40 Chen Y, Kelm RJ, Budd RC. et al. Augmentation of proliferation of vascular smooth muscle cells by plasminogen activator inhibitor type 1. Arterioscler Thrombos Vasc Biol 2006; 26: 1777-1783.
41 Budd RC. Death receptors couple to both cell proliferation and apoptosis. J Clin Invest 2002; 109: 437-441.
42 Kataoka T, Budd RC, Holler N. et al. The caspase-8 inhibitor FLIP promotes activation of NF-kappaB and Erk signaling pathways. Curr Biol 2000; 10: 640-648.