Effect of variations in the conserved residues E371 and S359 on the structural dynamics of protein Z dependent protease inhibitor (ZPI): a molecular dynamic simulation study

References

• Águila, S., Izaguirre, G., Martínez-Martínez, I., Vicente, V., Olson, S. T., & Corral, J. (2017). Disease-causing mutations in the serpin antithrombin reveal a key domain critical for inhibiting protease activities. The Journal of Biological Chemistry, 292 (40), 16513–16520. https://doi.org/10.1074/jbc.M117.787325
   PubMed Web of Science ®Google Scholar
• Bakan, A., Meireles, L. M., & Bahar, I. (2011). ProDy: Protein dynamics inferred from theory and experiments. Bioinformatics, 27(11), 1575–1577. https://doi.org/10.1093/bioinformatics/btr168
   PubMed Web of Science ®Google Scholar
• Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., Götz, A. W., Kolossváry, I., Wong, K. F., Paesani, F., … Kollma, P. A. (2012). AMBER 12. University of California.
   Google Scholar
• Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., & Baker, N. A. (2004). PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Research, 32(Web Server issue), W665–667. https://doi.org/10.1093/nar/gkh381
   PubMedGoogle Scholar
• Doncheva, N. T., Klein, K., Domingues, F. S., & Albrecht, M. (2011). Analyzing and visualizing residue networks of protein structures. Trends in Biochemical Sciences, 36(4), 179–182. https://doi.org/10.1016/j.tibs.2011.01.002
   PubMed Web of Science ®Google Scholar
• Emsley, P., Lohkamp, B., Scott, W. G., & Cowtan, K. (2010). Features and development of coot. Acta Crystallographica. Section D, Biological Crystallography, 66(Pt 4), 486–501. https://doi.org/10.1107/S0907444910007493
   PubMed Web of Science ®Google Scholar
• Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. Journal of Chemical Physics, 103(19), 8577–8593. https://doi.org/10.1063/1.470117
   Web of Science ®Google Scholar
• Gettins, P. G. W. (2002). Serpin structure, mechanism, and function. Chemical Reviews, 102(12), 4751–4803. https://doi.org/10.1021/cr010170+
   PubMed Web of Science ®Google Scholar
• Girard, T. J., Lasky, N. M., Grunz, K., & Broze, G. J J. (2019). Suppressing protein Z-dependent inhibition of factor Xa improves coagulation in hemophilia A. Journal of Thrombosis and Haemostasis, 17(1), 149–156. https://doi.org/10.1111/jth.14337
   PubMed Web of Science ®Google Scholar
• Han, X., Fiehler, R., & Broze, G. J., Jr. (2000). Characterization of the protein Z − dependent protease inhibitor. Blood, 96(9), 3049–3055. https://doi.org/10.1182/blood.V96.9.3049
   PubMed Web of Science ®Google Scholar
• Huang, X. (2019). Engineering a protein Z-dependent protease inhibitor (ZPI) mutant as a novel antagonist of ZPI anticoagulant function for hemophilia treatment. Journal of Thrombosis and Haemostasis, 17(10), 1655–1660. https://doi.org/10.1111/jth.14610
   PubMed Web of Science ®Google Scholar
• Huang, X., Dementiev, A., Olson, S. T., & Pg, G. (2010). Basis for the specificity and activation of the serpin protein Z-dependent proteinase inhibitor (ZPI) as an inhibitor of membrane-associated factor Xa. Journal of Biological Chemistry, 285 (26), 20399–20409.
   PubMed Web of Science ®Google Scholar
• Huang, X., Rezaie, A. R., Broze, G. J., & Olson, S. T. (2011). heparin is a major activator of the anticoagulant serpin, protein Z-dependent protease inhibitor. The Journal of Biological Chemistry, 286(11), 8740–8751. https://doi.org/10.1074/jbc.M110.188375
   PubMed Web of Science ®Google Scholar
• Huang, X., Swanson, R., Kroh, H. K., & Bock, P. E. (2019). Protein Z-dependent protease inhibitor (ZPI) is a physiologically significant inhibitor of prothrombinase function. The Journal of Biological Chemistry, 294(19), 7644–7657. https://doi.org/10.1074/jbc.RA118.006787
   PubMed Web of Science ®Google Scholar
• Huang, X., Yan, Y., Tu, Y., Gatti, J., Broze, G. J., Zhou, A., & Olson, S. T. (2012). Structural basis for catalytic activation of protein Z-dependent protease inhibitor (ZPI) by protein Z. Blood, 120(8), 1726–1733. https://doi.org/10.1182/blood-2012-03-419598
   PubMed Web of Science ®Google Scholar
• Huang, X., Zheng, Y., Zhang, F., Wei, Z., Wang, Y., Carrell, R. W., Read, R. J., Chen, G.-Q., & Zhou, A. (2016). Molecular mechanism of Z α1-antitrypsin deficiency. The Journal of Biological Chemistry, 291(30), 15674–15686. https://doi.org/10.1074/jbc.M116.727826
   PubMed Web of Science ®Google Scholar
• Huang, X., Zhou, J., Zhou, A., & Olson, S. T. (2015). Thermodynamic and kinetic characterization of the protein Z-dependent protease inhibitor (ZPI)-protein Z interaction reveals an unexpected role for ZPI Lys-239. The Journal of Biological Chemistry, 290(15), 9906–9918. https://doi.org/10.1074/jbc.M114.633479
   PubMed Web of Science ®Google Scholar
• Hughes, V. A., Meklemburg, R., Bottomley, S. P., & Wintrode, P. L. (2014). The Z mutation alters the global structural dynamics of α1-antitrypsin. PLoS One, 9(9), e102617. https://doi.org/10.1371/journal.pone.0102617
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD – Visual Molecular Dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Huntington, J. A. (2011). Serpin structure, function and dysfunction. Journal of Thrombosis and Haemostasis, 9, 26–34. https://doi.org/10.1111/j.1538-7836.2011.04360.x
   PubMed Web of Science ®Google Scholar
• Johnson, D. J., & Huntington, J. A. (2004). The influence of hinge region residue Glu-381 on antithrombin allostery and metastability. The Journal of Biological Chemistry, 279(6), 4913–4921. https://doi.org/10.1074/jbc.M311644200
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Kass, I., Knaupp, A. S., Bottomley, S. P., & Buckle, A. M. (2012). Conformational properties of the disease-causing Z variant of α1-antitrypsin revealed by theory and experiment . Biophysical Journal, 102 (12), 2856–2865. https://doi.org/10.1016/j.bpj.2012.05.023
   PubMed Web of Science ®Google Scholar
• Pasi, K. J., Rangarajan, S., Georgiev, P., Mant, T., Creagh, M. D., Lissitchkov, T., Bevan, D., Austin, S., Hay, C. R., Hegemann, I., Kazmi, R., Chowdary, P., Gercheva-Kyuchukova, L., Mamonov, V., Timofeeva, M., Soh, C.-H., Garg, P., Vaishnaw, A., Akinc, A., Sørensen, B., & Ragni, M. V. (2017). Targeting of antithrombin in hemophilia A or B with RNAi therapy. The New England Journal of Medicine, 377(9), 819–828. https://doi.org/10.1056/NEJMoa1616569
   PubMed Web of Science ®Google Scholar
• Patschull, A. O. M., Segu, L., Nyon, M. P., Lomas, D. A., Nobeli, I., Barrett, T. E., & Gooptu, B. (2011). Therapeutic target-site variability in α1-antitrypsin characterized at high resolution. Acta Crystallographica. Section F, Structural Biology and Crystallization Communications, 67(Pt 12), 1492–1497. https://doi.org/10.1107/S1744309111040267
   PubMedGoogle Scholar
• Peterson, J. A., Maroney, S. A., & Mast, A. E. (2016). Targeting TFPI for hemophilia treatment. Thrombosis Research, 141, S28–S30. https://doi.org/10.1016/S0049-3848(16)30359-0
   PubMed Web of Science ®Google Scholar
• Pike, R. N., Buckle, A. M., Le Bonniec, B. F., & Church, F. C. (2005). Control of the coagulation system by serpins getting by with a little help from glycosaminoglycans. The FEBS Journal, 272(19), 4842–4851. https://doi.org/10.1111/j.1742-4658.2005.04880.x
   PubMed Web of Science ®Google Scholar
• Piovesan, D., Minervini, G., & Tosatto, S. C. (2016). The RING 2.0 web server for high quality residue interaction networks. Nucleic Acids Research, 44(W1), W367–374. https://doi.org/10.1093/nar/gkw315
   PubMed Web of Science ®Google Scholar
• Polderdijk, S. G. I., Adams, T. E., Ivanciu, L., Camire, R. M., Baglin, T. P., & Huntington, J. A. (2017). Design and characterization of an APC-specific serpin for the treatment of hemophilia. Blood, 129(1), 105–113. https://doi.org/10.1182/blood-2016-05-718635
   PubMed Web of Science ®Google Scholar
• Prince, R., Bologna, L., Manetti, M., Melchiorre, D., Rosa, I., Dewarrat, N., Suardi, S., Amini, P., Fernández, J. A., Burnier, L., Quarroz, C., Reina Caro, M. D., Matsumura, Y., Kremer Hovinga, J. A., Griffin, J. H., Simon, H.-U., Ibba-Manneschi, L., Saller, F., Calzavarini, S., & Angelillo-Scherrer, A. (2018). Targeting anticoagulant protein S to improve hemostasis in hemophilia. Blood, 131 (12), 1360–1371. https://doi.org/10.1182/blood-2017-09-800326
   PubMed Web of Science ®Google Scholar
• Roe, D. R., & Cheatham, T. E. (2013). PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9(7), 3084–3095. https://doi.org/10.1021/ct400341p
   PubMed Web of Science ®Google Scholar
• Sengupta, T., & Manoj, N. (2016). Phosphatidylserine and phosphatidylethanolamine bind to protein Z cooperatively and with equal affinity. PLoS One, 11(9), e0161896. https://doi.org/10.1371/journal.pone.0161896
   PubMed Web of Science ®Google Scholar
• The PyMOL Molecular Graphics System Version 2.0, Schrodinger, LLC.
   Google Scholar
• Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general Amber force field. Journal of Computational Chemistry, 25(9), 1157–1174. https://doi.org/10.1002/jcc.20035
   PubMed Web of Science ®Google Scholar
• Wei, Z., Yan, Y., Carrell, R. W., & Zhou, A. (2009). Crystal structure of protein Z-dependent inhibitor complex shows how protein Z functions as a cofactor in the membrane inhibition of factor X. Blood, 114(17), 3662–3667. https://doi.org/10.1182/blood-2009-04-210021
   PubMed Web of Science ®Google Scholar
• Whisstock, J. C., Pike, R. N., Jin, L., Skinner, R., Pei, X. Y., Carrell, R. W., & Lesk, A. M. (2000). Conformational changes in serpins: II. The mechanism of activation of antithrombin by heparin. Journal of Molecular Biology, 301(5), 1287–1305. https://doi.org/10.1006/jmbi.2000.3982
   PubMed Web of Science ®Google Scholar
• Yang, L., Ding, Q., Huang, X., Olson, S. T., & Rezaie, A. R. (2012). Characterization of the heparin-binding site of the protein z-dependent protease inhibitor. Biochemistry, 51(19), 4078–4085. https://doi.org/10.1021/bi300353c
   PubMed Web of Science ®Google Scholar