Structural insight into inactivation of plasminogen activator inhibitor-1 by a small-molecule antagonist

Chemistry and Biology

Volumn 20, Issue 2, 2013, Pages 253-261

  Lin, Zhonghui ^a,b   Jensen, Jan K ^b   Hong, Zebin ^a,b   Shi, Xiaoli ^a,b   Hu, Lihong ^c   Andreasen, Peter A ^b   Huang, Mingdong ^a,b  

^a FUJIAN INSTITUTE OF RESEARCH ON THE STRUCTURE OF MATTER   (China)

^b AARHUS UNIVERSITY   (Denmark)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EMBELIN; PLASMINOGEN ACTIVATOR INHIBITOR 1;

ARTICLE; BINDING AFFINITY; DRUG BINDING SITE; DRUG DESIGN; DRUG IDENTIFICATION; ENZYME ACTIVITY; ENZYME INACTIVATION; MUTAGENESIS; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

BENZOQUINONES; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; KINETICS; MUTAGENESIS, SITE-DIRECTED; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN STRUCTURE, TERTIARY; SMALL MOLECULE LIBRARIES;

EID: 84874340538     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.01.002     Document Type: Article

References (66)

1. T. Abrahamsson, V. Nerme, M. Strömqvist, B. Akerblom, A. Legnehed, K. Pettersson, and A. Westin Eriksson Anti-thrombotic effect of a PAI-1 inhibitor in rats given endotoxin Thromb. Haemost. 75 1996 118 126
2. K.S. Ahn, G. Sethi, and B.B. Aggarwal Embelin, an inhibitor of X chromosome-linked inhibitor-of-apoptosis protein, blocks nuclear factor-κB (NF-κB) signaling pathway leading to suppression of NF-κB-regulated antiapoptotic and metastatic gene products Mol. Pharmacol. 71 2007 209 219
3. P.A. Andreasen PAI-1 - a potential therapeutic target in cancer Curr. Drug Targets 8 2007 1030 1041
4. M.B. Berkenpas, D.A. Lawrence, and D. Ginsburg Molecular evolution of plasminogen activator inhibitor-1 functional stability EMBO J. 14 1995 2969 2977
5. P. Björquist, J. Ehnebom, T. Inghardt, L. Hansson, M. Lindberg, M. Linschoten, M. Strömqvist, and J. Deinum Identification of the binding site for a low-molecular-weight inhibitor of plasminogen activator inhibitor type 1 by site-directed mutagenesis Biochemistry 37 1998 1227 1234
6. C.M. Blake, B.A. Sullenger, D.A. Lawrence, and Y.M. Fortenberry Antimetastatic potential of PAI-1-specific RNA aptamers Oligonucleotides 19 2009 117 128
7. N.A. Booth Fibrinolysis and thrombosis Best Pract. Res. Clin. Haematol. 12 1999 423 433
8. A.T. Brunger Version 1.2 of the Crystallography and NMR System Nature Protoc. 2 2007 2728 2733
9. J. Bryans, P. Charlton, I. Chicarelli-Robinson, M. Collins, R. Faint, C. Latham, I. Shaw, and S. Trew Inhibition of plasminogen activator inhibitor-1 activity by two diketopiperazines, XR330 and XR334 produced by Streptomyces sp J. Antibiot. 49 1996 1014 1021
10. J.M. Cale, S.H. Li, M. Warnock, E.J. Su, P.R. North, K.L. Sanders, M.M. Puscau, C.D. Emal, and D.A. Lawrence Characterization of a novel class of polyphenolic inhibitors of plasminogen activator inhibitor-1 J. Biol. Chem. 285 2010 7892 7902
11. P. Carmeliet, J.M. Stassen, L. Schoonjans, B. Ream, J.J. van den Oord, M. De Mol, R.C. Mulligan, and D. Collen Plasminogen activator inhibitor-1 gene-deficient mice. II. Effects on hemostasis, thrombosis, and thrombolysis J. Clin. Invest. 92 1993 2756 2760
12. R.W. Carrell, and P.E. Stein The biostructural pathology of the serpins: critical function of sheet opening mechanism Biol. Chem. Hoppe Seyler 377 1996 1 17
13. P.A. Charlton, R.W. Faint, F. Bent, J. Bryans, I. Chicarelli-Robinson, I. Mackie, S. Machin, and P. Bevan Evaluation of a low molecular weight modulator of human plasminogen activator inhibitor-1 activity Thromb. Haemost. 75 1996 808 815
14. Collaborative Computational Project 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D. Biol. Crystallogr. 50 1994 760 763
15. D.L. Crandall, H. Elokdah, L. Di, J.K. Hennan, N.V. Gorlatova, and D.A. Lawrence Characterization and comparative evaluation of a structurally unique PAI-1 inhibitor exhibiting oral in-vivo efficacy J. Thromb. Haemost. 2 2004 1422 1428
16. DeLano, W.L. (2003). The PyMOL Molecular Graphics System. http://www.pymol.org.
17. M.J. Duffy Urokinase plasminogen activator and its inhibitor, PAI-1, as prognostic markers in breast cancer: from pilot to level 1 evidence studies Clin. Chem. 48 2002 1194 1197
18. D.M. Dupont, J.B. Madsen, T. Kristensen, J.S. Bodker, G.E. Blouse, T. Wind, and P.A. Andreasen Biochemical properties of plasminogen activator inhibitor-1 Front. Biosci. 14 2009 1337 1361
19. R. Egelund, A.P. Einholm, K.E. Pedersen, R.W. Nielsen, A. Christensen, J. Deinum, and P.A. Andreasen A regulatory hydrophobic area in the flexible joint region of plasminogen activator inhibitor-1, defined with fluorescent activity-neutralizing ligands. Ligand-induced serpin polymerization J. Biol. Chem. 276 2001 13077 13086
20. A.P. Einholm, K.E. Pedersen, T. Wind, P. Kulig, M.T. Overgaard, J.K. Jensen, J.S. Bødker, A. Christensen, P. Charlton, and P.A. Andreasen Biochemical mechanism of action of a diketopiperazine inactivator of plasminogen activator inhibitor-1 Biochem. J. 373 2003 723 732
21. H. Elokdah, M. Abou-Gharbia, J.K. Hennan, G. McFarlane, C.P. Mugford, G. Krishnamurthy, and D.L. Crandall Tiplaxtinin, a novel, orally efficacious inhibitor of plasminogen activator inhibitor-1: design, synthesis, and preclinical characterization J. Med. Chem. 47 2004 3491 3494
22. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D. Biol. Crystallogr. 60 2004 2126 2132
23. 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 2002 491 496
24. 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 1990 74 76
25. P.W. Friederich, M. Levi, B.J. Biemond, P. Charlton, D. Templeton, A.J. van Zonneveld, P. Bevan, H. Pannekoek, and J.W. ten Cate Novel low-molecular-weight inhibitor of PAI-1 (XR5118) promotes endogenous fibrinolysis and reduces postthrombolysis thrombus growth in rabbits Circulation 96 1997 916 921
26. S.J. Gardell, J.A. Krueger, T.A. Antrilli, H. Elokdah, S. Mayer, S.J. Orcutt, D.L. Crandall, and G.P. Vlasuk Neutralization of plasminogen activator inhibitor I (PAI-1) by the synthetic antagonist PAI-749 via a dual mechanism of action Mol. Pharmacol. 72 2007 897 906
27. A. Gils, and P.J. Declerck The structural basis for the pathophysiological relevance of PAI-I in cardiovascular diseases and the development of potential PAI-I inhibitors Thromb. Haemost. 91 2004 425 437
28. A. Gils, J.M. Stassen, H. Nar, J.T. Kley, W. Wienen, U.J. Ries, and P.J. Declerck Characterization and comparative evaluation of a novel PAI-1 inhibitor Thromb. Haemost. 88 2002 137 143
29. J. Gliemann, A. Nykjaer, C.M. Petersen, K.E. Jørgensen, M. Nielsen, P.A. Andreasen, E.I. Christensen, A. Lookene, G. Olivecrona, and S.K. Moestrup The multiligand α2-macroglobulin receptor/low density lipoprotein receptor-related protein (α2MR/LRP). Binding and endocytosis of fluid phase and membrane-associated ligands Ann. N Y Acad. Sci. 737 1994 20 38
30. N.V. Gorlatova, J.M. Cale, H. Elokdah, D. Li, K. Fan, M. Warnock, D.L. Crandall, and D.A. Lawrence Mechanism of inactivation of plasminogen activator inhibitor-1 by a small molecule inhibitor J. Biol. Chem. 282 2007 9288 9296
31. 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 2001 6274 6283
32. L. Harris, H. Fritsche, R. Mennel, L. Norton, P. Ravdin, S. Taube, M.R. Somerfield, D.F. Hayes, R.C. Bast Jr. American Society of Clinical Oncology American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer J. Clin. Oncol. 25 2007 5287 5312
33. S.J. Harrop, L. Jankova, M. Coles, D. Jardine, J.S. Whittaker, A.R. Gould, A. Meister, G.C. King, B.C. Mabbutt, and P.M. Curmi The crystal structure of plasminogen activator inhibitor 2 at 2.0 A resolution: implications for serpin function Structure 7 1999 43 54
34. J.A. Huntington Shape-shifting serpins - advantages of a mobile mechanism Trends Biochem. Sci. 31 2006 427 435
35. Y. Izuhara, S. Takahashi, M. Nangaku, S. Takizawa, H. Ishida, K. Kurokawa, C. van Ypersele de Strihou, N. Hirayama, and T. Miyata Inhibition of plasminogen activator inhibitor-1: its mechanism and effectiveness on coagulation and fibrosis Arterioscler. Thromb. Vasc. Biol. 28 2008 672 677
36. F. Jänicke, A. Prechtl, C. Thomssen, N. Harbeck, C. Meisner, M. Untch, C.G. Sweep, H.K. Selbmann, H. Graeff, M. Schmitt German N0 Study Group Randomized adjuvant chemotherapy trial in high-risk, lymph node-negative breast cancer patients identified by urokinase-type plasminogen activator and plasminogen activator inhibitor type 1 J. Natl. Cancer Inst. 93 2001 913 920
37. J.K. Jensen, and P.G. Gettins High-resolution structure of the stable plasminogen activator inhibitor type-1 variant 14-1B in its proteinase-cleaved form: a new tool for detailed interaction studies and modeling Protein Sci. 17 2008 1844 1849
38. J.K. Jensen, T. Wind, and P.A. Andreasen The vitronectin binding area of plasminogen activator inhibitor-1, mapped by mutagenesis and protection against an inactivating organochemical ligand FEBS Lett. 521 2002 91 94
39. J.K. Jensen, A. Malmendal, B. Schiøtt, S. Skeldal, K.E. Pedersen, L. Celik, N.C. Nielsen, P.A. Andreasen, and T. Wind Inhibition of plasminogen activator inhibitor-1 binding to endocytosis receptors of the low-density-lipoprotein receptor family by a peptide isolated from a phage display library Biochem. J. 399 2006 387 396
40. E.K. Kruithof, M.S. Baker, and C.L. Bunn Biological and clinical aspects of plasminogen activator inhibitor type 2 Blood 86 1995 4007 4024
41. R.A. Laskowski, D.S. Moss, and J.M. Thornton Main-chain bond lengths and bond angles in protein structures J. Mol. Biol. 231 1993 1049 1067
42. E.G. Levin, and L. Santell Conversion of the active to latent plasminogen activator inhibitor from human endothelial cells Blood 70 1987 1090 1098
43. A. Liang, F. Wu, K. Tran, S.W. Jones, G. Deng, B. Ye, Z. Zhao, R.M. Snider, W.P. Dole, J. Morser, and Q. Wu Characterization of a small molecule PAI-1 inhibitor, ZK4044 Thromb. Res. 115 2005 341 350
44. Z. Lin, L. Jiang, C. Yuan, J.K. Jensen, X. Zhang, Z. Luo, B.C. Furie, B. Furie, P.A. Andreasen, and M. Huang Structural basis for recognition of urokinase-type plasminogen activator by plasminogen activator inhibitor-1 J. Biol. Chem. 286 2011 7027 7032
45. M.P. Look, W.L. van Putten, M.J. Duffy, N. Harbeck, I.J. Christensen, C. Thomssen, R. Kates, F. Spyratos, M. Fernö, and S. Eppenberger-Castori Pooled analysis of prognostic impact of urokinase-type plasminogen activator and its inhibitor PAI-1 in 8377 breast cancer patients J. Natl. Cancer Inst. 94 2002 116 128
46. J.B. Madsen, D.M. Dupont, T.B. Andersen, A.F. Nielsen, L. Sang, D.M. Brix, J.K. Jensen, T. Broos, M.L. Hendrickx, and A. Christensen RNA aptamers as conformational probes and regulatory agents for plasminogen activator inhibitor-1 Biochemistry 49 2010 4103 4115
47. S. Mahendran, S. Badami, and V. Maithili Evaluation of antidiabetic effect of embelin from Embelia ribes in alloxan induced diabetes in rats Biomed. Prev. Nutr. 1 2010 25 31
48. L. Mathiasen, D.M. Dupont, A. Christensen, G.E. Blouse, J.K. Jensen, A. Gils, P.J. Declerck, T. Wind, and P.A. Andreasen A peptide accelerating the conversion of plasminogen activator inhibitor-1 to an inactive latent state Mol. Pharmacol. 74 2008 641 653
49. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D. Biol. Crystallogr. 53 1997 240 255
50. H. Nar, M. Bauer, J.M. Stassen, D. Lang, A. Gils, and P.J. Declerck Plasminogen activator inhibitor 1. Structure of the native serpin, comparison to its other conformers and implications for serpin inactivation J. Mol. Biol. 297 2000 683 695
51. J. Neve, P.A. Leone, A.R. Carroll, R.W. Moni, N.J. Paczkowski, G. Pierens, P. Björquist, J. Deinum, J. Ehnebom, and T. Inghardt Sideroxylonal C, a new inhibitor of human plasminogen activator inhibitor type-1, from the flowers of Eucalyptus albens J. Nat. Prod. 62 1999 324 326
52. L.S. Nielsen, P.A. Andreasen, J. Grøndahl-Hansen, J.Y. Huang, P. Kristensen, and K. Danø Monoclonal antibodies to human 54,000 molecular weight plasminogen activator inhibitor from fibrosarcoma cells - inhibitor neutralization and one-step affinity purification Thromb. Haemost. 55 1986 206 212
53. Z. Nikolovska-Coleska, L. Xu, Z. Hu, Y. Tomita, P. Li, P.P. Roller, R. Wang, X. Fang, R. Guo, and M. Zhang Discovery of embelin as a cell-permeable, small-molecular weight inhibitor of XIAP through structure-based computational screening of a traditional herbal medicine three-dimensional structure database J. Med. Chem. 47 2004 2430 2440
54. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
55. K.E. Pedersen, A.P. Einholm, A. Christensen, L. Schack, T. Wind, J.M. Kenney, and P.A. Andreasen Plasminogen activator inhibitor-1 polymers, induced by inactivating amphipathic organochemical ligands Biochem. J. 372 2003 747 755
56. S. Reuter, S. Prasad, K. Phromnoi, R. Kannappan, V.R. Yadav, and B.B. Aggarwal Embelin suppresses osteoclastogenesis induced by receptor activator of NF-κB ligand and tumor cells in vitro through inhibition of the NF-κB cell signaling pathway Mol. Cancer Res. 8 2010 1425 1436
57. A. Rupin, R. Gaertner, P. Mennecier, I. Richard, A. Benoist, G. De Nanteuil, and T.J. Verbeuren S35225 is a direct inhibitor of Plasminogen Activator Inhibitor type-1 activity in the blood Thromb. Res. 122 2008 265 270
58. D. Seiffert, and D.J. Loskutoff Evidence that type 1 plasminogen activator inhibitor binds to the somatomedin B domain of vitronectin J. Biol. Chem. 266 1991 2824 2830
59. A.M. Sharp, P.E. Stein, N.S. Pannu, R.W. Carrell, M.B. Berkenpas, D. Ginsburg, D.A. Lawrence, and R.J. Read The active conformation of plasminogen activator inhibitor 1, a target for drugs to control fibrinolysis and cell adhesion Structure 7 1999 111 118
60. P. Stein, and C. Chothia Serpin tertiary structure transformation J. Mol. Biol. 221 1991 615 621
61. M.P. Stoppelli, L.M. Andersen, and G. Votta Engineered antagonists of uPA and PAI-1 D. Edwards, G. Høyer-Hansen, F. Blasi, B.F. Sloane, The Cancer Degradome - Proteases and Cancer Biology 2008 Springer New York 721 758
62. T.J. Stout, H. Graham, D.I. Buckley, and D.J. Matthews Structures of active and latent PAI-1: a possible stabilizing role for chloride ions Biochemistry 39 2000 8460 8469
63. J.J. van Giezen, G. Wahlund, Nerme, and T. Abrahamsson The Fab-fragment of a PAI-1 inhibiting antibody reduces thrombus size and restores blood flow in a rat model of arterial thrombosis Thromb. Haemost. 77 1997 964 969
64. D.E. Vaughan Angiotensin and vascular fibrinolytic balance Am. J. Hypertens. 15 2002 3S 8S
65. A. Zhou, R. Faint, P. Charlton, T.R. Dafforn, R.W. Carrell, and D.A. Lomas Polymerization of plasminogen activator inhibitor-1 J. Biol. Chem. 276 2001 9115 9122
66. A. Zhou, J.A. Huntington, N.S. Pannu, R.W. Carrell, and R.J. Read How vitronectin binds PAI-1 to modulate fibrinolysis and cell migration Nat. Struct. Biol. 10 2003 541 544