Small molecule inhibitors of plasminogen activator inhibitor-1 elicit anti-Tumorigenic and anti-Angiogenic activity

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Placencio, Veronica R ^a,b   Ichimura, Atsuhiko ^c   Miyata, Toshio ^c   DeClerck, Yves A ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CHILDREN S HOSPITAL LOS ANGELES   (United States)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 [2 [2 (4 BENZHYDRYLPIPERAZIN 1 YL) 2 OXOETHOXY]ACETAMIDO] 5 CHLOROBENZOIC ACID; 5 CHLORO 2 [[[2 [[3 (FURAN 3 YL)PHENYL]AMINO]2 OXOETHOXY]ACETYL]AMINO]BENZOIC ACID; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 7; UNCLASSIFIED DRUG; 4 AMINOBENZOIC ACID DERIVATIVE; 5-CHLORO-2-(((2-(4-(DIPHENYLMETHYL)PIPERAZIN-1-YL)-2-OXOETHOXY)ACETYL)AMINO)BENZOATE; PIPERAZINE DERIVATIVE; PLASMINOGEN ACTIVATOR INHIBITOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG STRUCTURE; ENDOTHELIUM CELL; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IC50; IN VIVO STUDY; MAXIMUM PLASMA CONCENTRATION; MOUSE; NONHUMAN; SURVIVAL RATE; TUMOR VASCULARIZATION; ANIMAL; CARCINOGENESIS; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; TUMOR CELL LINE;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOGENESIS; CELL LINE, TUMOR; CELL SURVIVAL; ENDOTHELIAL CELLS; MICE; PARA-AMINOBENZOATES; PIPERAZINES; PLASMINOGEN ACTIVATOR INHIBITOR 1;

EID: 84941636578     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133786     Document Type: Article

References (37)

1. Declerck PJ, Gils A. Three decades of research on plasminogen activator inhibitor-1: A multifaceted serpin. Semin Thromb Hemost. 2013; 39:356-64. doi:10.1055/s-0033-1334487 PMID: 23504606.
2. McMahon B, Kwaan HC. The plasminogen activator system and cancer. Pathophysiol Haemost Thromb. 2008; 36:184-94. doi:10.1159/000175156 PMID: 19176991.
3. VanDeCraen B, Declerck PJ, Gils A. The Biochemistry, Physiology and Pathological roles of PAI-1 and the requirements for PAI-1 inhibition in vivo. Thromb Res. 2012; 130:576-85. doi:10.1016/j.thromres.2012.06.023 PMID: 22801256.
4. Binder BR, Mihaly J. The plasminogen activator inhibitor "paradox" in cancer. Immunol Lett. 2008; 118:116-24. doi:10.1016/j.imlet.2008.03.017 PMID: 18495253.
5. Foekens JA, Peters HA, Look MP, Portengen H, Schmitt M, Kramer MD, et al. The urokinase system of plasminogen activation and prognosis in 2780 breast cancer patients. Cancer Res. 2000; 60:636-43. PMID: 10676647.
6. Bajou K, Masson V, Gerard RD, Schmitt PM, Albert V, Praus M, et al. The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin. Implications for antiangiogenic strategies. J Cell Biol. 2001; 152:777-84. PMID: 11266468.
7. Isogai C, Laug WE, Shimada H, Declerck PJ, Stins MF, Durden DL, et al. Plasminogen activator inhibitor- 1 promotes angiogenesis by stimulating endothelial cell migration toward fibronectin. Cancer Res. 2001; 61:5587-94. PMID: 11454712.
8. Bajou K, Peng H, Laug WE, Maillard C, Noel A, Foidart JM, et al. Plasminogen activator inhibitor-1 protects endothelial cells from FasL-mediated apoptosis. Cancer Cell. 2008; 14:324-34. doi:10.1016/j.ccr.2008.08.012 PMID: 18835034.
9. Bajou K, Noel A, Gerard RD, Masson V, Brunner N, Holst-Hansen C, et al. Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat Med. 1998; 4:923-8. PMID: 9701244.
10. Fang H, Placencio VR, De Clerck YA. Protumorigenic activity of plasminogen activator inhibitor-1 through an antiapoptotic function. J Natl Cancer Inst. 2012; 104:1470-84. doi:10.1093/jnci/djs377 PMID: 22984202.
11. Elokdah H, Abou-Gharbia M, Hennan JK, McFarlane G, Mugford CP, Krishnamurthy G, et al. Tiplaxtinin, a novel, orally efficacious inhibitor of plasminogen activator inhibitor-1: design, synthesis, and preclinical characterization. J Med Chem. 2004; 47:3491-4. PMID: 15214776.
12. Gomes-Giacoia E, Miyake M, Goodison S, Rosser CJ. Targeting plasminogen activator inhibitor-1 inhibits angiogenesis and tumor growth in a human cancer xenograft model. Mol Cancer Ther. 2013; 12:2697-708. doi:10.1158/1535-7163.MCT-13-0500 PMID: 24072883.
13. Gorlatova NV, Cale JM, Elokdah H, Li D, Fan K, Warnock M, et al. Mechanism of inactivation of plasminogen activator inhibitor-1 by a small molecule inhibitor. J Biol Chem. 2007; 282:9288-96. PMID: 17276980.
14. Izuhara Y, Takahashi S, Nangaku M, Takizawa S, Ishida H, Kurokawa K, et al. Inhibition of plasminogen activator inhibitor-1: its mechanism and effectiveness on coagulation and fibrosis. Arterioscler Thromb Vasc Biol. 2008; 28:672-7. doi:10.1161/ATVBAHA.107.157479 PMID: 18239154.
15. Izuhara Y, Yamaoka N, Kodama H, Dan T, Takizawa S, Hirayama N, et al. A novel inhibitor of plasminogen activator inhibitor-1 provides antithrombotic benefits devoid of bleeding effect in nonhuman primates. J Cereb Blood Flow Metab. 2010; 30:904-12. doi:10.1038/jcbfm.2009.272 PMID: 20087372.
16. Huang WT, Vayalil PK, Miyata T, Hagood J, Liu RM. Therapeutic value of small molecule inhibitor to plasminogen activator inhibitor-1 for lung fibrosis. Am J Respir Cell Mol Biol. 2012; 46:87-95. doi:10.1165/rcmb.2011-0139OC PMID: 21852684.
17. Boe AE, Eren M, Murphy SB, Kamide CE, Ichimura A, Terry D, et al. Plasminogen activator inhibitor-1 antagonist TM5441 attenuates Nomega-nitro-L-arginine methyl ester-induced hypertension and vascular senescence. Circulation. 2013; 128:2318-24. doi:10.1161/CIRCULATIONAHA.113.003192 PMID: 24092817.
18. Pelisch N, Dan T, Ichimura A, Sekiguchi H, Vaughan DE, van Ypersele de Strihou C, et al. Plasminogen Activator Inhibitor-1 Antagonist TM5484 Attenuates Demyelination and Axonal Degeneration in a Mice Model of Multiple Sclerosis. PLoS One. 2015; 10:e0124510. doi:10.1371/journal.pone.0124510 PMID: 25915660.
19. Mashiko S, Kitatani K, Toyoshima M, Ichimura A, Dan T, Usui T, et al. Inhibition of plasminogen activator inhibitor-1 is a potential therapeutic strategy in ovarian cancer. Cancer Biol Ther. 2015:0.
20. Yamaoka N, Kodama H, Izuhara Y, Miyata T, Meguro K. Structure-activity relationships of new N-acylanthranilic acid derivatives as plasminogen activator inhibitor-1 inhibitors. Chem Pharm Bull (Tokyo). 2011; 59:215-24.
21. Mouchess ML, Sohara Y, Nelson MD Jr, De CYA, Moats RA. Multimodal imaging analysis of tumor progression and bone resorption in a murine cancer model. J Comput Assist Tomogr. 2006; 30:525-34. PMID: 16778634.
22. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N. Computer control of microscopes using micro- Manager. Curr Protoc Mol Biol. 2010;Chapter 14:Unit14 20.
23. Team RC. A language and environment for statistical computing. Vienna, Austria. 2014. Available: http://www.R-project.org/.
24. StataCorp. Stat Statistical Software: Release 11. 2009.
25. Schneider DJ, Chen Y, Sobel BE. The effect of plasminogen activator inhibitor type 1 on apoptosis. Thromb Haemost. 2008; 100:1037-40. PMID: 19132227.
26. Balsara RD, Ploplis VA. Plasminogen activator inhibitor-1: The double-edged sword in apoptosis. Thromb Haemost. 2008; 100:1029-36. PMID: 19132226.
27. Zoellner H, Hofler M, Beckmann R, Bielek E, Vanyek E, Kumabashiri I, et al. Fibrinolytic proteins in apoptotic human umbilical vein endothelial cells. Thromb Res. 1998; 91:209-19. PMID: 9755833.
28. 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; 281:22527-36. PMID: 16785241.
29. Chen Y, Kelm RJ Jr, Budd RC, Sobel BE, Schneider DJ. Inhibition of apoptosis and caspase-3 in vascular smooth muscle cells by plasminogen activator inhibitor type-1. J Cell Biochem. 2004; 92:178-88. PMID: 15095413.
30. Rossignol P, Luttun A, Martin-Ventura JL, Lupu F, Carmeliet P, Collen D, et al. Plasminogen activation: A mediator of vascular smooth muscle cell apoptosis in atherosclerotic plaques. J Thromb Haemost. 2006; 4:664-70. PMID: 16460449.
31. Lademann UA, Romer MU. Regulation of programmed cell death by plasminogen activator inhibitor type 1 (PAI-1). Thromb Haemost. 2008; 100:1041-6. PMID: 19132228.
32. Placencio VR, DeClerck YA. Plasminogen Activator Inhibitor-1 in Cancer: Rationale and Insight for Future Therapeutic Testing. Cancer Research. 2015.
33. Masuda T, Hattori N, Senoo T, Akita S, Ishikawa N, Fujitaka K, et al. SK-216, an inhibitor of plasminogen activator inhibitor-1, limits tumor progression and angiogenesis. Mol Cancer Ther. 2013; 12:2378- 88. doi:10.1158/1535-7163.MCT-13-0041 PMID: 23990114.
34. Fortenberry YM. Plasminogen activator inhibitor-1 inhibitors: A patent review (2006-present). Expert Opin Ther Pat. 2013; 23:801-15. doi:10.1517/13543776.2013.782393 PMID: 23521527.
35. Iwaki T, Nagahashi K, Kobayashi T, Umemura K, Terao T, Kanayama N. The first report of uncontrollable subchorionic and retroplacental haemorrhage inducing preterm labour in complete PAI-1 deficiency in a human. Thromb Res. 2012; 129:e161-3. doi:10.1016/j.thromres.2011.10.008 PMID: 22099705.
36. Vercauteren E, Peeters M, Hoylaerts MF, Lijnen HR, Meijers JC, Declerck PJ, et al. The hyperfibrinolytic state of mice with combined thrombin-activatable fibrinolysis inhibitor (TAFI) and plasminogen activator inhibitor-1 gene deficiency is critically dependent on TAFI deficiency. J Thromb Haemost. 2012; 10:2555-62. doi:10.1111/jth.12036 PMID: 23083123.
37. Fay WP, Parker AC, Condrey LR, Shapiro AD. Human plasminogen activator inhibitor-1 (PAI-1) deficiency: characterization of a large kindred with a null mutation in the PAI-1 gene. Blood. 1997; 90:204- 8. PMID: 9207454.