Zafirlukast is a broad-spectrum thiol isomerase inhibitor that inhibits thrombosis without altering bleeding times

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Atwood, B. K., Lopez, J., Wager-Miller, J., Mackie, K., & Straiker, A. (2011). Expression of G protein-coupled receptors and related proteins in HEK293, AtT20, BV2, and N18 cell lines as revealed by microarray analysis. BMC Genomics, 12, 14. doi:10.1186/1471-2164-12-14 Bekendam, R. H., Bendapudi, P. K., Lin, L., Nag, P. P., Pu, J., Kennedy, D. R., . . . Flaumenhaft, R. (2016). A substrate-driven allosteric switch that enhances PDI catalytic activity. Nat Commun, 7, 12579. doi:10.1038/ncomms12579 Bi, S., Hong, P. W., Lee, B., & Baum, L. G. (2011). Galectin-9 binding to cell surface protein disulfide isomerase regulates the redox environment to enhance T-cell migration and HIV entry. Proceedings of the National Academy of Sciences of the United States of America, 108(26), 10650-10655. doi:10.1073/pnas.1017954108 Cho, J., Furie, B. C., Coughlin, S. R., & Furie, B. (2008). A critical role for extracellular protein disulfide isomerase during thrombus formation in mice. The Journal of clinical investigation, 118(3), 1123-1131. Cho, J., Kennedy, D. R., Lin, L., Huang, M., Merrill-Skoloff, G., Furie, B. C., & Furie, B. (2012). Protein disulfide isomerase capture during thrombus formation in vivo depends on the presence of beta3 integrins. Blood, 120(3), 647-655. doi:10.1182/blood-2011-08-372532 Dekhuijzen, P. N., & Koopmans, P. P. (2002). Pharmacokinetic profile of zafirlukast. Clin Pharmacokinet, 41(2), 105-114. doi:10.2165/00003088-200241020-00003 Essex, D. W., & Li, M. (1999a). Protein disulphide isomerase mediates platelet aggregation and secretion. British journal of haematology, 104(3), 448-454. Essex, D. W., & Li, M. (1999b). Protein disulphide isomerase mediates platelet aggregation and secretion. British journal of haematology, 104(3), 448-454. Falati, S., Patil, S., Gross, P. L., Stapleton, M., Merrill-Skoloff, G., Barrett, N. E., . . . Gibbins, J. M. (2006). Platelet PECAM-1 inhibits thrombus formation in vivo. Blood, 107(2), 535-541. doi:10.1182/blood-2005-04-1512 Figueroa, E. E., Kramer, M., Strange, K., & Denton, J. S. (2019). CysLT1 receptor antagonists Pranlukast and Zafirlukast inhibit LRRC8-mediated volume regulated anion channels independently of the receptor. Am J Physiol Cell Physiol. doi:10.1152/ajpcell.00281.2019 Fischer, J. D., Song, M. H., Suttle, A. B., Heizer, W. D., Burns, C. B., Vargo, D. L., & Brouwer, K. L. (2000). Comparison of zafirlukast (Accolate) absorption after oral and colonic administration in humans. Pharmaceutical research, 17(2), 154-159. doi:10.1023/a:1007509112383 Furie, B., & Furie, B. C. (2012). Formation of the clot. Thromb Res, 130 Suppl 1, S44-46. doi:10.1016/j.thromres.2012.08.272 Gobel, T., Diehl, O., Heering, J., Merk, D., Angioni, C., Wittmann, S. K., . . . Kahnt, A. S. (2019). Zafirlukast Is a Dual Modulator of Human Soluble Epoxide Hydrolase and Peroxisome Proliferator-Activated Receptor gamma. Front Pharmacol, 10, 263. doi:10.3389/fphar.2019.00263 Goplen, D., Wang, J., Enger, P. O., Tysnes, B. B., Terzis, A. J., Laerum, O. D., & Bjerkvig, R. (2006). Protein disulfide isomerase expression is related to the invasive properties of malignant glioma. Cancer research, 66(20), 9895-9902. Hasegawa, S., Ichiyama, T., Hashimoto, K., Suzuki, Y., Hirano, R., Fukano, R., & Furukawa, S. (2010). Functional expression of cysteinyl leukotriene receptors on human platelets. Platelets, 21(4), 253-259. doi:10.3109/09537101003615394 Holbrook, L. M., Sandhar, G. K., Sasikumar, P., Schenk, M. P., Stainer, A. R., Sahli, K. A., . . . Gibbins, J. M. (2018). A humanized monoclonal antibody that inhibits platelet-surface ERp72 reveals a role for ERp72 in thrombosis. Journal of thrombosis and haemostasis : JTH, 16(2), 367-377. doi:10.1111/jth.13878 Holbrook, L. M., Sasikumar, P., Stanley, R. G., Simmonds, A. D., Bicknell, A. B., & Gibbins, J. M. (2012). The platelet-surface thiol isomerase enzyme ERp57 modulates platelet function. Journal of thrombosis and haemostasis : JTH, 10(2), 278-288. doi:10.1111/j.1538-7836.2011.04593.x Holbrook, L. M., Watkins, N. A., Simmonds, A. D., Jones, C. I., Ouwehand, W. H., & Gibbins, J. M. (2009). Platelets release novel thiol isomerase enzymes which are recruited to the cell surface following activation. British journal of haematology. Holmgren, A. (1979). Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. The Journal of biological chemistry, 254(19), 9627-9632. Hussmann, M., Janke, K., Kranz, P., Neumann, F., Mersch, E., Baumann, M., . . . Metzen, E. (2015). Depletion of the thiol oxidoreductase ERp57 in tumor cells inhibits proliferation and increases sensitivity to ionizing radiation and chemotherapeutics. Oncotarget, 6(36), 39247-39261. doi:10.18632/oncotarget.5746 Jasuja, R., Passam, F. H., Kennedy, D. R., Kim, S. H., van Hessem, L., Lin, L., . . . Flaumenhaft, R. (2012). Protein disulfide isomerase inhibitors constitute a new class of antithrombotic agents. J Clin Invest, 122(6), 2104-2113. doi:10.1172/JCI61228 Jordan, P. A., Stevens, J. M., Hubbard, G. P., Barrett, N. E., Sage, T., Authi, K. S., & Gibbins, J. M. (2005). A role for the thiol isomerase protein ERP5 in platelet function. Blood, 105(4), 1500-1507. Kilkenny, C., Browne, W., Cuthill, I. C., Emerson, M., Altman, D. G., & Group, N. C. R. R. G. W. (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. J Gene Med, 12(7), 561-563. doi:10.1002/jgm.1473 Kim, K., Hahm, E., Li, J., Holbrook, L. M., Sasikumar, P., Stanley, R. G., . . . Cho, J. (2013). Platelet protein disulfide isomerase is required for thrombus formation but not for hemostasis in mice. Blood, 122(6), 1052-1061. doi:10.1182/blood-2013-03-492504 Lahav, J., Jurk, K., Hess, O., Barnes, M. J., Farndale, R. W., Luboshitz, J., & Kehrel, B. E. (2002). Sustained integrin ligation involves extracellular free sulfhydryls and enzymatically catalyzed disulfide exchange. Blood, 100(7), 2472-2478. Laidlaw, T. M., & Boyce, J. A. (2012). Cysteinyl leukotriene receptors, old and new; implications for asthma. Clin Exp Allergy, 42(9), 1313-1320. doi:10.1111/j.1365-2222.2012.03982.x Lau, W. K., Chow, A. W., Au, S. C., & Ko, W. H. (2011). Differential inhibitory effects of CysLT(1) receptor antagonists on P2Y(6) receptor-mediated signaling and ion transport in human bronchial epithelia. PloS one, 6(7), e22363. doi:10.1371/journal.pone.0022363 Lawrence, D. A., Song, R., & Weber, P. (1996). Surface thiols of human lymphocytes and their changes after in vitro and in vivo activation. Journal of leukocyte biology, 60(5), 611-618. doi:10.1002/jlb.60.5.611 Li, S., Li, C., Ryu, H. H., Lim, S. H., Jang, W. Y., & Jung, S. (2016). Bacitracin Inhibits the Migration of U87-MG Glioma Cells via Interferences of the Integrin Outside-in Signaling Pathway. J Korean Neurosurg Soc, 59(2), 106-116. doi:10.3340/jkns.2016.59.2.106 Li, S., Zhao, X., Chang, S., Li, Y., Guo, M., & Guan, Y. (2019). ERp57small interfering RNA silencing can enhance the sensitivity of drugresistant human ovarian cancer cells to paclitaxel. International journal of oncology, 54(1), 249-260. doi:10.3892/ijo.2018.4628 Lin, C. Y., Hu, C. T., Cheng, C. C., Lee, M. C., Pan, S. M., Lin, T. Y., & Wu, W. S. (2016). Oxidation of heat shock protein 60 and protein disulfide isomerase activates ERK and migration of human hepatocellular carcinoma HepG2. Oncotarget, 7(10), 11067-11082. doi:10.18632/oncotarget.7093 Mamedova, L., Capra, V., Accomazzo, M. R., Gao, Z. G., Ferrario, S., Fumagalli, M., . . . Jacobson, K. A. (2005). CysLT1 leukotriene receptor antagonists inhibit the effects of nucleotides acting at P2Y receptors. Biochemical pharmacology, 71(1-2), 115-125. doi:10.1016/j.bcp.2005.10.003 Michie, A. J., Zintel, H. A., & et al. (1949). The nephrotoxicity of bacitracin in man. Surgery, 26(4), 626-632. Moraes, L. A., Spyridon, M., Kaiser, W. J., Jones, C. I., Sage, T., Atherton, R. E., & Gibbins, J. M. (2010). Non-genomic effects of PPARgamma ligands: inhibition of GPVI-stimulated platelet activation. Journal of thrombosis and haemostasis : JTH, 8(3), 577-587. doi:10.1111/j.1538-7836.2009.03732.x Nguyen, T. M., Muhammad, S. A., Ibrahim, S., Ma, L., Guo, J., Bai, B., & Zeng, B. (2018). DeCoST: A New Approach in Drug Repurposing From Control System Theory. Front Pharmacol, 9, 583. doi:10.3389/fphar.2018.00583 Passam, F. H., Lin, L., Gopal, S., Stopa, J. D., Bellido-Martin, L., Huang, M., . . . Furie, B. (2015). Both platelet- and endothelial cell-derived ERp5 support thrombus formation in a laser-induced mouse model of thrombosis. Blood, 125(14), 2276-2285. doi:10.1182/blood-2013-12-547208 Piromkraipak, P., Sangpairoj, K., Tirakotai, W., Chaithirayanon, K., Unchern, S., Supavilai, P., . . . Vivithanaporn, P. (2018). Cysteinyl Leukotriene Receptor Antagonists Inhibit Migration, Invasion, and Expression of MMP-2/9 in Human Glioblastoma. Cell Mol Neurobiol, 38(2), 559-573. doi:10.1007/s10571-017-0507-z Popielarski, M., Ponamarczuk, H., Stasiak, M., Watala, C., & Swiatkowska, M. (2019). Modifications of disulfide bonds in breast cancer cell migration and invasiveness. Am J Cancer Res, 9(8), 1554-1582. Robinson, A., O'Neill, S., Kiernan, A., O'Donoghue, N., & Moran, N. (2006). Bacitracin reveals a role for multiple thiol isomerases in platelet function. British journal of haematology, 132(3), 339-348. Samanta, S., Tamura, S., Dubeau, L., Mhawech-Fauceglia, P., Miyagi, Y., Kato, H., . . . Neamati, N. (2017). Expression of protein disulfide isomerase family members correlates with tumor progression and patient survival in ovarian cancer. Oncotarget, 8(61), 103543-103556. doi:10.18632/oncotarget.21569 Smith, A. M., Chan, J., Oksenberg, D., Urfer, R., Wexler, D. S., Ow, A., . . . Huang, S. G. (2004). A high-throughput turbidometric assay for screening inhibitors of protein disulfide isomerase activity. Journal of biomolecular screening, 9(7), 614-620. doi:10.1177/1087057104265292 Stopa, J. D., Neuberg, D., Puligandla, M., Furie, B., Flaumenhaft, R., & Zwicker, J. I. (2017). Protein disulfide isomerase inhibition blocks thrombin generation in humans by interfering with platelet factor V activation. JCI Insight, 2(1), e89373. doi:10.1172/jci.insight.89373 Tanaka, L. Y., Araujo, T. L. S., Rodriguez, A. I., Ferraz, M. S., Pelegati, V. B., Morais, M. C. C., . . . Laurindo, F. R. M. (2019). Peri/epicellular protein disulfide isomerase-A1 acts as an upstream organizer of cytoskeletal mechanoadaptation in vascular smooth muscle cells. American journal of physiology. Heart and circulatory physiology, 316(3), H566-H579. doi:10.1152/ajpheart.00379.2018 VerPlank, L., Khodier, C., Nag, P. P., Pu, J., Wurst, J., Pilyugina, T., . . . Schrieber, S. L. (2013). Identification of ML359 as a Small Molecule Inhibitor of Protein Disulfide Isomerase Probe Reports from the NIH Molecular Libraries Program. Bethesda (MD). Wang, L., Wu, Y., Zhou, J., Ahmad, S. S., Mutus, B., Garbi, N., . . . Essex, D. W. (2013). Platelet-derived ERp57 mediates platelet incorporation into a growing thrombus by regulation of the alphaIIbbeta3 integrin. Blood. doi:10.1182/blood-2013-06-506691 Wu, Y., Ahmad, S. S., Zhou, J., Wang, L., Cully, M. P., & Essex, D. W. (2012). The disulfide isomerase ERp57 mediates platelet aggregation, hemostasis, and thrombosis. Blood, 119(7), 1737-1746. doi:10.1182/blood-2011-06-360685 Xu, S., Butkevich, A. N., Yamada, R., Zhou, Y., Debnath, B., Duncan, R., . . . Neamati, N. (2012). Discovery of an orally active small-molecule irreversible inhibitor of protein disulfide isomerase for ovarian cancer treatment. Proceedings of the National Academy of Sciences of the United States of America, 109(40), 16348-16353. doi:10.1073/pnas.1205226109 Xu, S., Liu, Y., Yang, K., Wang, H., Shergalis, A., Kyani, A., . . . Neamati, N. (2019). Inhibition of protein disulfide isomerase in glioblastoma causes marked downregulation of DNA repair and DNA damage response genes. Theranostics, 9(8), 2282-2298. doi:10.7150/thno.30621 Yang, S., Shergalis, A., Lu, D., Kyani, A., Liu, Z., Ljungman, M., & Neamati, N. (2019). Design, Synthesis, and Biological Evaluation of Novel Allosteric Protein Disulfide Isomerase Inhibitors. J Med Chem, 62(7), 3447-3474. doi:10.1021/acs.jmedchem.8b01951 Ye, Q., Fu, P., Dou, J., & Wang, N. (2018). Downregulation of PDIA3 inhibits proliferation and invasion of human acute myeloid leukemia cells. Onco Targets Ther, 11, 2925-2935. doi:10.2147/OTT.S162407 Zhou, J., Wu, Y., Chen, F., Wang, L., Rauova, L., Hayes, V. M., . . . Essex, D. W. (2017). The disulfide isomerase ERp72 supports arterial thrombosis in mice. Blood, 130(6), 817-828. doi:10.1182/blood-2016-12-755587 Zhou, J., Wu, Y., Wang, L., Rauova, L., Hayes, V. M., Poncz, M., & Essex, D. W. (2015). The C-terminal CGHC motif of protein disulfide isomerase supports thrombosis. The Journal of clinical investigation, 125(12), 4391-4406. doi:10.1172/JCI80319 Zhou, X., Cai, J., Liu, W., Wu, X., & Gao, C. (2019). Cysteinyl leukotriene receptor type 1 (CysLT1R) antagonist zafirlukast protects against TNF-alpha-induced endothelial inflammation. Biomed Pharmacother, 111, 452-459. doi:10.1016/j.biopha.2018.12.064 Zwicker, J. I., Schlechter, B. L., Stopa, J. D., Liebman, H. A., Aggarwal, A., Puligandla, M., . . . Investigators, C. (2019). Targeting protein disulfide isomerase with the flavonoid isoquercetin to improve hypercoagulability in advanced cancer. JCI Insight, 4(4). doi:10.1172/jci.insight.125851