Maximal PAI-1 inhibition in vivo requires neutralizing antibodies that recognize and inhibit glycosylated PAI-1

Thrombosis Research

Volumn 129, Issue 4, 2012, Pages

  Van De Craen, Britt ^a   Scroyen, Ilse ^b   Vranckx, Christine ^b   Compernolle, Griet ^a   Lijnen, H Roger ^b   Declerck, Paul J ^a   Gils, Ann ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Endotoxemia model; Glycosylation; Monoclonal antibodies; Mouse PAI 1

Indexed keywords

LIPOPOLYSACCHARIDE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 124K1; MONOCLONAL ANTIBODY 33H1F7; MONOCLONAL ANTIBODY H4B3; MONOCLONAL ANTIBODY MP2D2; NEUTRALIZING ANTIBODY; PLASMINOGEN ACTIVATOR INHIBITOR 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; DEGLYCOSYLATION; EMBRYO; ENDOTOXEMIA; ENZYME INHIBITION; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN GLYCOSYLATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ENDOTOXEMIA; GLYCOSYLATION; MICE; MICE, INBRED BALB C; PLASMINOGEN ACTIVATOR INHIBITOR 1;

EID: 84858333034     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/j.thromres.2011.11.038     Document Type: Article

References (60)

1. D.C. Rijken, and H.R. Lijnen New insights into the molecular mechanisms of the fibrinolytic system J Thromb Haemost 7 1 2009 4 13
2. H.J. Ehrlich, R.K. Gebbink, J. Keijer, M. Linders, K.T. Preissner, and H. Pannekoek Alteration of serpin specificity by a protein cofactor-vitronectin endows plasminogen activator inhibitor-1 with thrombin inhibitory properties J Biol Chem 265 22 1990 13029 13035
3. H. Pannekoek, H. Veerman, H. Lambers, P. Diergaarde, C.L. Verweij, and A.J. Vanzonneveld Endothelial plasminogen activator inhibitor (PAI): a new member of the Serpin gene family EMBO J 5 10 1986 2539 2544
4. A.J. Simpson, N.A. Booth, N.R. Moore, and B. Bennett Distribution of plasminogen activator inhibitor (PAI-1) in tissues J Clin Pathol 44 2 1991 139 143
5. A. Gils, and P.J. Declerck Structure-function relationships in serpins: Current concepts and controversies Thromb Haemost 80 4 1998 531 541
6. E.K.O. Kruithof Plasminogen activator inhibitor type 1: Biochemical, biological and clinical aspects Fibrinolysis 2 Supp. 2 1988 59 70
7. P.J. Declerck, M. Demol, M.C. Alessi, S. Baudner, E.P. Paques, and K.T. Preissner Purification and characterization of a plasminogen activator inhibitor-1 binding protein from human plasma-Identification as a multimeric form of S-protein (vitronectin) J Biol Chem 263 30 1988 15454 15461
8. A. Gils, K.E. Pedersen, P. Skottrup, A. Christensen, D. Naessens, and J. Deinum Biochemical importance of glycosylation of plasminogen activator inhibitor-I Thromb Haemost 90 2 2003 206 217
9. D. Lawrence, L. Strandberg, T. Grundstrom, and T. Ny Purification of active human plasminogen activator inhibitor-1 from Escherichia coli-comparison with natural and recombinant forms purified from eukaryotic cells Eur J Biochem 186 3 1989 523 533
10. D.M. Dupont, J.B. Madsen, T. Kristensen, J.S. Bodker, G.E. Blouse, and T. Wind Biochemical properties of plasminogen activator inhibitor-1 Front Biosci 14 2009 1337 1361
11. A. Hamsten, B. Wiman, U. Defaire, and M. Blomback Increased plasma levels of a rapid inhibitor of tissue plasminogen activator in young survivors of myocardial infraction N Engl J Med 313 25 1985 1557 1563
12. A. Hamsten, U. Defaire, G. Walldius, G. Dahlen, A. Szamosi, and C. Landou Plasminogen activator inhibitor in plasma - risk factor for recurrent myocardial infarction Lancet 2 8549 1987 3 8
13. A.M. Thogersen, J.H. Jansson, K. Boman, T.K. Nilsson, L. Weinehall, and F. Huhtasaari High plasminogen activator inhibitor and tissue plasminogen activator levels in plasma precede a first acute myocardial infarction in both men and women - Evidence for the fibrinolytic system as an independent primary risk factor Circulation 98 21 1998 2241 2247
14. I. Juhan-Vague, J. Valadier, M. Alessi, M. Aillaud, J. Ansaldi, and C. Philip Joet Deficient t-PA release and elevated PA inhibitor levels in patients with spontaneous or recurrent deep venous thrombosis Thromb Haemost 57 1987 67 72
15. M.E. Meltzer, T. Lisman, P.G. de Groot, J.C.M. Meijers, S. le Cessie, and C.J.M. Doggen Venous thrombosis risk associated with plasma hypofibrinolysis is explained by elevated plasma levels of TAFI and PAI-1 Blood 116 1 2010 113 121
16. N. Garg, and W.P. Fay Plasminogen activator inhibitor-1 and Restenosis Curr Drug Targets 8 2007 1003 1006
17. S. Konstantinides, K. Schafer, and D.J. Loskutoff Do PAI-1 and vitronectin promote or inhibit neointima formation? The exact role of the fibrinolytic system in vascular remodeling remains uncertain Arterioscler Thromb Vasc Biol 22 12 2002 1943 1945
18. B.R. Binder, and J. Mihaly The plasminogen activator inhibitor "paradox" in cancer Immunol Lett 118 2 2008 116 124
19. J. Schneiderman, M.S. Sawdey, M.R. Keeton, G.M. Bordin, E.F. Bernstein, and R.B. Dilley Increased type-1 plasminogen activator inhibitor gene expression in atherosclerotic human arteries Proc Natl Acad Sci U S A 89 15 1992 6998 7002
20. F. Lupu, G.E. Bergonzelli, D.A. Heim, E. Cousin, C.Y. Genton, and F. Bachmann Localization and production of plasminogen activator inhibitor-1 in human healthy and atherosclerotic arteries Arterioscler Thromb 13 7 1993 1090 1100
21. L.A. Erickson, G.J. Fici, J.E. Lund, T.P. Boyle, H.G. Polites, and K.R. Marotti Development of venous occlusions in mice transgenic for the plasminogen activator inhibitor-1 gene Nature 346 6279 1990 74 76
22. M. Eren, C.A. Painter, J.B. Atkinson, P.J. Declerck, and D.E. Vaughan Age-dependent spontaneous coronary arterial thrombosis in transgenic mice that express a stable form of human plasminogen activator inhibitor-1 Circulation 106 4 2002 491 496
23. P. Carmeliet, J.M. Stassen, L. Schoonjans, B. Ream, J.J. Vandenoord, and M. Demol Plasminogen activator inhibitor-1 gene deficient mice. II. Effects on hemostasis, thrombosis and thrombolysis J Clin Invest 92 6 1993 2756 2760
24. S. Stefansson, G.A. McMahon, E. Petitclerc, and D.A. Lawrence Plasminogen activator inhibitor-1 in tumor growth, angiogenesis and vascular remodeling Curr Pharm Des 9 19 2003 1545 1564
25. C. Dellas, and D.J. Loskutoff Historical analysis of PAI-1 from its discovery to its potential role in cell motility and disease Thromb Haemost 93 2005 631 640 (Epub March 7, 2005)
26. H.R. Lijnen Pleiotropic functions of plasminogen activator inhibitor-1 J Thromb Haemost 3 1 2005 35 45
27. S. Debrock, and P.J. Declerck Neutralization of plasminogen activator inhibitor-1 inhibitory properties: Identification of two different mechanisms Biochim Biophys Acta Protein Struct Mol Enzymol 1337 2 1997 257 266
28. L.S. Nielsen, P.A. Andreasen, J. Grondahlhansen, J.Y. Huang, P. Kristensen, and K. Dano Monoclonal antibodies to human 54,000 molecular weight plasminogen activator inhibitor from fibrosarcoma cells-inhibitor neutralization and one-step affinity purification Thromb Haemost 55 2 1986 206 212
29. J. Keijer, M. Linders, A.J. Vanzonneveld, H.J. Ehrlich, J.P. Deboer, and H. Pannekoek The interaction of plasminogen activator inhibitor-1 with plasminogen activators (tissue-type and urokinase-type) and fibrin - Localization of interaction sites and physiological relevance Blood 78 2 1991 401 409
30. P.J. Declerck, and D. Collen Measurement of plasminogen activator inhibitor-1 (PAI-1) in plasma with various monoclonal antibody-based enzyme-linked immunosorbent assays Thromb Res 1990 3 9
31. D.M. Dupont, G.E. Blouse, M. Hansen, L. Mathiasen, S. Kjelgaard, and J.K. Jensen Evidence for a pre-latent form of the serpin plasminogen activator inhibitor-1 with a detached beta-strand 1C J Biol Chem 281 47 2006 36071 36081
32. P. Carmeliet, L. Kieckens, L. Schoonjans, B. Ream, A. Vannuffelen, and G. Prendergast Plasminogen activator inhibitor-1 gene deficient mice. I. Generation by homologeous recombination and characterization J Clin Invest 92 6 1993 2746 2755
33. P.J. Declerck, M. Verstreken, and D. Collen Immunoassay of murine t-PA, u-PA and PAI-1 using monoclonal antibodies raised in gene-inactivated mice Thromb Haemost 74 5 1995 1305 1309
34. T. Kawasaki, M. Dewerchin, H.R. Lijnen, J. Vermylen, and M.F. Hoylaerts Vascular release of plasminogen activator inhibitor-1 impairs fibrinolysis during acute arterial thrombosis in mice Blood 96 1 2000 153 160
35. M. Hansen, M.N. Busse, and P.A. Andreasen Importance of the amino-acid composition of the shutter region of plasminogen activator inhibitor-1 for its transitions to latent and substrate forms Eur J Biochem 268 23 2001 6274 6283
36. A.P. Bijnens, A. Gils, I. Knockaert, J.M. Stassen, and P.J. Declerck Importance of the hinge region between alpha-helix F and the main part of serpins, based upon identification of the epitope of plasminogen activator inhibitor type 1 neutralizing antibodies J Biol Chem 275 9 2000 6375 6380
37. J.H. Verheijen, G.T.G. Chang, and C. Kluft Evidence for the occurence of a fast-acting inhibitor for tissue-type plasminogen activator in human plasma Thromb Haemost 51 3 1984 392 395
38. K. Verbeke, A. Gils, and P.J. Declerck Inhibition of plasminogen activator inhibitor-1: antibody fragments and their unique sequences as a tool for the development of profibrinolytic drugs J Thromb Haemost 2 2 2004 298 305
39. R. Javed, K. Yarimizu, N. Pelletier, C. Li, and A.F. Knowles Mutagenesis of lysine 62, asparagine 64, and conserved region 1 reduces the activity of human ecto-ATPase (NTPDase 2) Biochemistry 46 22 2007 6617 6627
40. A. Kern, A.I. Agoulnik, and G.D. Bryant-Greenwood The low-density lipoprotein class a module of the relaxin receptor (leucine-rich repeat containing G-protein coupled receptor 7): Its role in signaling and trafficking to the cell membrane Endocrinology 148 3 2007 1181 1194
41. M.F. Tansky, C. Pothoulakis, and S.E. Leeman Functional consequences of alteration of N-linked glycosylation sites on the neurokinin 1 receptor Proc Natl Acad Sci U S A 104 25 2007 10691 10696
42. B. Van De Craen, I. Scroyen, R. Abdelnabi, E. Brouwers, H.R. Lijnen, and P.J. Declerck Characterization of a panel of monoclonal antibodies toward mouse PAI-1 that exert a significant profibrinolytic effect in vivo Thromb Res 128 2011 68 76
43. T.H. Ngo, M.F. Hoylaerts, I. Knockaert, E. Brouwers, and P.J. Declerck Identification of a target site in plasminogen activator inhibitor-1 that allows neutralization of its inhibitory properties concomitant with an allosteric up-regulation of its antiadhesive properties J Biol Chem 276 28 2001 26243 26248
44. T.H. Ngo, and P.J. Declerck Suppression of plasminogen activator inhibitor 1 (PAI-1) activity levels in rats by monoclonal antibodies Fibrinolysis Proteolysis 12 6 1998 335 339
45. A. Gils, L.M. Meissenheimer, G. Compernolle, and P.J. Declerck Species-dependent molecular drug targets in plasminogen activator inhibitor-1 (PAI-1) Thromb Haemost 102 3 2009 609 610
46. C. Roca, L. Primo, D. Vaidembri, A. Cividalli, P. Declerck, and P. Carmeliet Hyperthermia inhibits angiogenesis by a plasminogen activator inhibitor 1-dependent mechanism Can Res 63 7 2003 1500 1507
47. N.V. Gorlatova, H. Elokdah, K. Fan, D.L. Crandall, and D.A. Lawrence Mapping of a conformational epitope on plasminogen activator inhibitor-1 by random mutagenesis - Implications for serpin function J Biol Chem 278 18 2003 16329 16335
48. L. Kjoller, P.M. Martensen, L. SottrupJensen, J. Justesen, K.W. Rodenburg, and P.A. Andreasen Conformational changes of the reactive-centre loop and beta-strand 5A accompany temperature-dependent inhibitor-substrate transition of plasminogen-activator inhibitor 1 Eur J Biochem 241 1 1996 38 46
49. M.C. Alessi, P.J. Declerck, M. Demol, L. Nelles, and D. Collen Purification and characterization of natural and recombinant human plasminogen activator inhibitor-1 (PAI-1) Eur J Biochem 175 3 1988 531 540
50. K.W. Rodenburg, L. Kjoller, H.H. Petersen, and P.A. Andreasen Binding of urokinase-type plasminogen activator plasminogen activator inhibitor-1 complex to the endocytosis receptors alpha(2)-macroglobulin receptor low-density lipoprotein receptor-related protein and very-low-density lipoprotein receptor involves basic residues in the inhibitor Biochem J 329 1998 55 63
51. A. Gils, I. Knockaert, and P.J. Declerck Substrate behavior of plasminogen activator inhibitor-1 is not associated with a lack of insertion of the reactive site loop Biochemistry 35 23 1996 7474 7481
52. A. Gils, I. Knockaert, E. Brouwers, and P.J. Declerck Glycosylation dependent conformational transitions in plasminogen activator inhihitor-1: evidence for the presence of two active conformations Fibrinolysis Proteolysis 14 1 2000 58 64
53. P.A. Andreasen, R. Egelund, S. Jensen, and K.W. Rodenburg Solvent effects on activity and conformation of plasminogen activator inhibitor-1 Thromb Haemost 81 3 1999 407 414
54. C.N. Berry, C. Lunven, I. Lechaire, C. Girardot, and S.E. O'Connor Antithrombotic activity of a monoclonal antibody inducing the substrate form of plasminogen activator inhibitor type 1 in rat models of venous and arterial thrombosis Br J Pharmacol 125 1 1998 29 34
55. J.K. Hennan, G.A. Morgan, R.E. Swillo, T.M. Antrilli, C. Mugford, and G.P. Vlasuk Effect of tiplaxtinin (PAI-039), an orally bioavailable PAI-1 antagonist, in a rat model of thrombosis J Thromb Haemost 6 9 2008 1558 1564
56. J. Mestas, and C.C.W. Hughes Of mice and not men: Differences between mouse and human immunology J Immunol 172 5 2004 2731 2738
57. H.R. Lijnen, B. Vanhoef, V. Beelen, and D. Collen Characterization of the murine plasma fibrinolytic system Eur J Biochem 224 3 1994 863 871
58. I. Scroyen, V. Christiaens, and H.R. Lijnen No functional role of plasminogen activator inhibitor-1 in murine adipogenesis or adipocyte differentiation J Thromb Haemost 5 1 2007 139 145
59. H. Brogren, C. Sihlbom, K. Wallmark, M. Lonn, J. Deinum, and L. Karlsson Heterogeneous glycosylation patterns of human PAI-1 may reveal its cellular origin Thromb Res 122 2 2008 271 281
60. A. Helenius, and M. Aebi Intracellular functions of N-linked glycans Science 291 5512 2001 2364 2369