785
Views
21
CrossRef citations to date
0
Altmetric
Research Articles

Molecular dynamics simulations of aptamer-binding reveal generalized allostery in thrombin

& (Jr)
Pages 3354-3369 | Received 18 Jul 2016, Accepted 21 Oct 2016, Published online: 29 Nov 2016

References

  • Abdi, H., & Williams, L. J. (2010). Principal component analysis. Wiley Interdisciplinary Reviews: Computational Statistics, 2, 433–459. doi:10.1002/wics.101
  • Adams, T. E., & Huntington, J. A. (2006). Thrombin-cofactor interactions: Structural insights into regulatory mechanisms. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, 1738–1745. doi:10.1161/01.ATV.0000228844.65168.d1
  • Akhavan, S., Mannucci, P. M., Lak, M., Mancuso, G., Mazzucconi, M. G., Rocino, A., … Perkins, S. J. (2000). Identification and three-dimensional structural analysis of nine novel mutations in patients with prothrombin deficiency. Thrombosis and Haemostasis, 84, 989–997.
  • Article, R., Steering, I., For, C., & Thrombosis, W. (2014). Thrombosis: A major contributor to the global disease burden. Journal of Thrombosis and Haemostasis, 12, 1580–1590. doi:10.1111/jth.12698
  • Baglin, T. P., Carrell, R. W., Church, F. C., Esmon, C. T., & Huntington, J. A. (2002). Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism. Proceedings of the National Academy of Sciences, 99, 11079–11084. doi:10.1073/pnas.162232399
  • Bajzar, L., Morser, J., & Nesheim, M. (1996). TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex. Journal of Biological Chemistry, 271, 16603–16608. doi:10.1074/jbc.271.28.16603
  • Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81, 3684–3690. doi:10.1063/1.448118
  • Blombäck, B., Hessel, B., Hogg, D., & Therkildsen, L. (1978). A two-step fibrinogen–fibrin transition in blood coagulation. Nature, 275, 501–505. doi:10.1038/275501a0
  • Bode, W. (2006). Structure and interaction modes of thrombin. Blood Cells, Molecules & Diseases, 36, 122–130. doi:10.1016/j.bcmd.2005.12.027
  • Bosshard, H. R. (2001, August). Molecular recognition by induced fit: how fit is the concept? News in Physiological Sciences : An International Journal of Physiology Produced Jointly by the International Union of Physiological Sciences and the American Physiological Society, 16, 171–173.
  • Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., … Karplus, M. (2009). CHARMM: The biomolecular simulation program. Journal of Computational Chemistry, 30, 1545–1614. doi:10.1002/jcc.21287
  • Carter, I. S. R., Vanden Hoek, A. L., Pryzdial, E. L. G., & MacGillivray, R. T. A. (2010). Thrombin A-chain: Activation remnant or allosteric effector? Thrombosis, 2010, 1–9. doi:10.1155/2010/416167
  • Changeux, J.-P., & Edelstein, S. (2011). Conformational selection or induced fit? 50 years of debate resolved. F1000 Biology Reports, 3, 19–35. doi:10.3410/B3-19
  • Colwell, N. S., Blinder, M. A., Tsiang, M., Gibbs, C. S., Bock, P. E., & Tollefsen, D. M. (1998). Allosteric effects of a monoclonal antibody against thrombin exosite II. Biochemistry, 37, 15057–15065. doi:10.1021/bi980925f
  • Coughlin, S. R. (2000). Thrombin signalling and protease-activated receptors. Nature, 407, 258–264. doi:10.1038/35025229
  • Crawley, J. T. B., Zanardelli, S., Chion, C. K. N. K., & Lane, D. A. (2007). The central role of thrombin in hemostasis. Journal of Thrombosis and Haemostasis, 5, 95–101. doi:10.1111/j.1538-7836.2007.02500.x
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98, 10089–10092. doi:10.1063/1.464397
  • Davie, E., & Kulman, J. (2006). An overview of the structure and function of thrombin. Seminars in Thrombosis and Hemostasis, 32, 003–015. http://doi.org/10.1055/s-2006-939550
  • Di Cera, E. (2008). Thrombin. Molecular Aspects of Medicine, 29, 203–254. doi:10.1016/j.mam.2008.01.001
  • Erdmann, J. (2010). Engineered thrombin aims to take on heparin. Chemistry and Biology, 17, 1267–1268. doi:10.1016/j.chembiol.2010.12.005
  • Feenstra, K. A., Hess, B., & Berendsen, H. J. C. (1999). Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems. Journal of Computational Chemistry, 20, 786–798. doi:10.1002/(SICI)1096-987X(199906)20:8<786:AID-JCC5>3.0.CO;2-B
  • Figueiredo, A. C., Clement, C. C., Zakia, S., Gingold, J., Philipp, M., & Pereira, P. J. B. (2012). Rational design and characterization of D-Phe-Pro-D-Arg-derived direct thrombin inhibitors. PLoS ONE, 7. doi:10.1371/journal.pone.0034354.
  • Fredenburgh, J. C., Stafford, A. R., & Weitz, J. I. (1997). Evidence for allosteric linkage between exosites 1 and 2 of thrombin. Journal of Biological Chemistry, 272, 25493–25499.10.1074/jbc.272.41.25493
  • Godwin, R. C., Melvin, R., & Salsbury, F. R. (2015). Molecular dynamics simulations and computer-aided drug discovery. In Wei Zhang (Ed.), Computer-aided drug discovery (pp. 1–30). New York: Springer. doi:10.1007/7653_2015_41
  • Godwin, R., Gmeiner, W., & Salsbury, F. R. (2016). Importance of long-time simulations for rare event sampling in zinc finger proteins. Journal of Biomolecular Structure and Dynamics, 34, 125–134. doi:10.1080/07391102.2015.1015168
  • van Gunsteren, W. F., & Berendsen, H. J. C. (1977). Algorithms for macromolecular dynamics and constraint dynamics. Molecular Physics, 34, 1311–1327. doi:10.1080/00268977700102571
  • Häggström, O. (2002). Finite Markov chains and algorithmic applications (Vol. 52). Cambridge: Society. doi:10.1017/CBO9780511613586
  • Harvey, M. J., & De Fabritiis, G. (2009). An implementation of the smooth particle mesh Ewald method on GPU hardware. Journal of Chemical Theory and Computation, 5, 2371–2377. doi:10.1021/ct900275y
  • Harvey, M. J., Giupponi, G., & De Fabritiis, G. (2009). ACEMD: Accelerating biomolecular dynamics in the microsecond time scale. Journal of Chemical Theory and Computation, 5, 1632–1639. doi:10.1021/ct9000685
  • Hayward, S., Kitao, A., & Go, N. (1994). Harmonic and anharmonic aspects in the dynamics of BPTI: A normal mode analysis and principal component analysis. Protein Science : A Publication of the Protein Society, 3, 936–943. doi:10.1002/pro.5560030608
  • Heyer, L. J., Kruglyak, S., & Yooseph, S. (1999). Exploring expression data: Identification and analysis of coexpressed genes. Genome Research, 9, 1106–1115. doi:10.1101/gr.9.11.1106
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 33–38. doi:10.1016/0263-7855(96)00018-5
  • Huntington, J. A. (2008). How Na+ activates thrombin – A review of the functional and structural data. Biological Chemistry, 389, 1025–1035. doi:10.1515/BC.2008.113
  • Huntington, J. A. (2012). Thrombin plasticity. Biochimica et Biophysica Acta, 1824, 246–252. doi:10.1016/j.bbapap.2011.07.005
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics. doi:10.1063/1.445869
  • Keefe, A. D., Pai, S., & Ellington, A. (2010). Aptamers as therapeutics. Nature Reviews. Drug Discovery, 9, 537–550. doi:10.1038/nrd3141
  • Knaggs, M. H., Salsbury, F. R., Edgell, M. H., & Fetrow, J. S. (2007). Insights into correlated motions and long-range interactions in CheY derived from molecular dynamics simulations. Biophysical Journal, 92, 2062–2079. doi:10.1529/biophysj.106.081950
  • Lefkowitz, J. B., Haver, T., Clarke, S., Jacobson, L., Weller, A., Nuss, R., … Hathaway, W. E. (2000). The prothrombin Denver patient has two different prothrombin point mutations resulting in Glu-300–>Lys and Glu-309–>Lys substitutions. British Journal of Haematology, 108, 182–187. doi:bjh1810 [pii].
  • Lemons, D. S. (1997). Paul Langevin’s 1908 paper “On the Theory of Brownian Motion” [“Sur la théorie du mouvement brownien,” C. R. Acad. Sci. (Paris) 146, 530–533 (1908)]. American Journal of Physics,, 65, 1079–1081. doi:10.1119/1.18725
  • Levy, R. M., Srinivasan, A. R., Olson, W. K., & McCammon, J. A. (1984). Quasi-harmonic method for studying very low frequency modes in proteins. Biopolymers, 23, 1099–1112. doi:10.1002/bip.360230610
  • Li, W., Johnson, D. J. D., Esmon, C. T., & Huntington, J. A. (2004). Structure of the antithrombin-thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nature Structural & Molecular Biology, 11, 857–862. doi:10.1038/nsmb811
  • Li, W., Wang, K., Zhao, M., Yang, X., Chen, M., & Lan, X. (2014). Development of aptamer oligonucleotides as anticoagulants and antithrombotics for cardiovascular diseases: Current status. Thrombosis Research, 134, 769–773. doi:10.1016/j.thromres.2014.05.021
  • Liaw, P. C., Fredenburgh, J. C., Stafford, A. R., Tulinsky, A., Austin, R. C., & Weitz, J. I. (1998). Localization of the thrombin-binding domain on prothrombin fragment 2. Journal of Biological Chemistry, 273, 8932–8939.10.1074/jbc.273.15.8932
  • McCammon, J. A., Gelin, B. R., & Karplus, M. (1977). Dynamics of folded proteins. Nature, 267, 585–590. doi:10.1038/267585a0
  • Melnikova, I. (2009). The anticoagulants market. Nature Reviews. Drug Discovery, 8, 353–353. doi:10.1038/nrd2851
  • Melvin, R., & Salsbury, F. (2015). VisualStatistics. Figshare. doi:10.6084/m9.figshare.1601897
  • Melvin, R., & Salsbury, F. (2016). Python implementation of quality threshold clustering for molecular dynamics. Figshare. doi:10.6084/m9.figshare.3813930.v2
  • Melvin, R. L., & Salsbury, F. R. (2016). Visualizing ensembles in structural biology. Journal of Molecular Graphics and Modelling, 67, 44–53. doi:10.1016/j.jmgm.2016.05.001
  • Melvin, R., Godwin, R., Xiao, J., & Salsbury, F. (2015). Markov cluster analysis in matlab. Figshare. doi:10.6084/m9.figshare.1566809
  • Motlagh, H. N., Wrabl, J. O., Li, J., & Hilser, V. J. (2014). The ensemble nature of allostery. Nature, 508, 331–339. doi:10.1038/nature13001
  • Negureanu, L., & Salsbury, F. R. (2012). Insights into protein – DNA interactions, stability and allosteric communications: A computational study of Mutsα-DNA recognition complexes. Journal of Biomolecular Structure and Dynamics, 29, 757–776. doi:10.1080/07391102.2012.10507412
  • Negureanu, L., & Salsbury, F. R. (2014). Non-specificity and synergy at the binding site of the carboplatin-induced DNA adduct via molecular dynamics simulations of the MutSα-DNA recognition complex. Journal of Biomolecular Structure & Dynamics, 32, 969–992. doi:10.1080/07391102.2013.799437
  • Nelson-Piercy, C. (1997). 6 Hazards of heparin: Allergy, heparin-induced thrombocytopenia and osteoporosis. Baillière’s Clinical Obstetrics and Gynaecology, 11, 489–509. doi:10.1016/S0950-3552(97)80024-7
  • Ni, X., Castanares, M., Mukherjee, A., & Lupold, S. E. (2011). Nucleic acid aptamers: Clinical applications and promising new horizons. Current Medicinal Chemistry, 18, 4206–4214. doi:10.2174/092986711797189600
  • Nierodzik, M. L., & Karpatkin, S. (2006). Thrombin induces tumor growth, metastasis, and angiogenesis: Evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell, 10, 355–362. doi:10.1016/j.ccr.2006.10.002
  • Nimjee, S. M., Oney, S., Volovyk, Z., Bompiani, K. M., Long, S. B., Hoffman, M., & Sullenger, B. A. (2009). Synergistic effect of aptamers that inhibit exosites 1 and 2 on thrombin. RNA (New York, N.Y.), 15, 2105–2111. doi:10.1261/rna.1240109
  • Opalinska, J. B., & Gewirtz, A. M. (2002, July). Nucleic-acid therapeutics: Basic principles and recent applications. Nature Reviews. Drug Discovery, 1, 503–514. doi:10.1038/nrd837
  • Padmanabhan, K., & Tulinsky, A. (1996). An ambiguous structure of a DNA 15-mer thrombin complex. Acta Crystallographica Section D, Biological Crystallography, 52, 272–282. doi:10.1107/S0907444995013977
  • Padmanabhan, K., Padmanabhan, K. P., Ferrara, J. D., Sadler, J. E., & Tulinsky, A. (1993). The structure of alpha-thrombin inhibited by a 15-mer single-stranded DNA aptamer. The Journal of Biological Chemistry, 268, 17651–17654.
  • Papaconstantinou, M. E., Bah, A., & Di Cera, E. (2008). Role of the A chain in thrombin function. Cellular and Molecular Life Sciences, 65, 1943–1947. doi:10.1007/s00018-008-8179-y
  • Petrera, N. S., Stafford, A. R., Leslie, B. A., Kretz, C. A., Fredenburgh, J. C., & Weitz, J. I. (2009). long range communication between exosites 1 and 2 modulates thrombin function. Journal of Biological Chemistry, 284, 25620–25629. doi:10.1074/jbc.M109.000042
  • Pozzi, N., Chen, R., Chen, Z., Bah, A., & Di Cera, E. (2011). Rigidification of the autolysis loop enhances Na+ binding to thrombin. Biophysical Chemistry, 159, 6–13. doi:10.1016/j.bpc.2011.04.003
  • Radjabi, A. R., Sawada, K., Jagadeeswaran, S., Eichbichler, A., Kenny, H. A., Montag, A., … Lengyel, E. (2008). Thrombin induces tumor invasion through the induction and association of matrix metalloproteinase-9 and  1-integrin on the cell surface. Journal of Biological Chemistry, 283, 2822–2834. doi:10.1074/jbc.M704855200
  • Russo Krauss, I., Merlino, A., Randazzo, A., Novellino, E., Mazzarella, L., & Sica, F. (2012). High-resolution structures of two complexes between thrombin and thrombin-binding aptamer shed light on the role of cations in the aptamer inhibitory activity. Nucleic Acids Research, 40, 8119–8128. doi:10.1093/nar/gks512
  • Šali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234, 779–815. doi:10.1006/jmbi.1993.1626
  • Salomon-Ferrer, R., Case, D. A., & Walker, R. C. (2013). An overview of the Amber biomolecular simulation package. Wiley Interdisciplinary Reviews: Computational Molecular Science, 3, 198–210. doi:10.1002/wcms.1121
  • Salsbury, F. R., Crowder, M. W., Kingsmore, S. F., & Huntley, J. J. A. (2009). Molecular dynamic simulations of the metallo-beta-lactamase from Bacteroides fragilis in the presence and absence of a tight-binding inhibitor. Journal of Molecular Modeling, 15, 133–145. doi:10.1007/s00894-008-0410-0
  • Salsbury, F. R., Yuan, Y., Knaggs, M. H., Poole, L. B., & Fetrow, J. S. (2012). Structural and electrostatic asymmetry at the active site in typical and atypical peroxiredoxin dimers. The Journal of Physical Chemistry. B, 116, 6832–6843. doi:10.1021/jp212606k
  • Salsbury, F. R. (2010). Molecular dynamics simulations of protein dynamics and their relevance to drug discovery. Current Opinion in Pharmacology, 10, 738–744. doi:10.1016/j.coph.2010.09.016
  • Scherer, M. K., Trendelkamp-Schroer, B., Paul, F., Pérez-Hernández, G., Hoffmann, M., Plattner, N., … Noé, F. (2015). PyEMMA 2: A software package for estimation, validation, and analysis of Markov models. Journal of Chemical Theory and Computation, 11, 5525–5542. doi:10.1021/acs.jctc.5b00743
  • van der Spuy, W. J., & Pretorius, E. (2012). Interrelation between inflammation, thrombosis, and neuroprotection in cerebral ischemia. Reviews in the Neurosciences, 23, 269–278. doi:10.1515/revneuro-2012-0028
  • Takagi, T., & Doolittle, R. F. (1974). Amino acid sequence studies on factor XIII and the peptide released during its activation by thrombin. Biochemistry, 13, 750–756.10.1021/bi00701a018
  • Tanaka, K. A., Key, N. S., & Levy, J. H. (2009). Blood coagulation: Hemostasis and thrombin regulation. Anesthesia and Analgesia, 108, 1433–1446. doi:10.1213/ane.0b013e31819bcc9c
  • Tsai, C.-J., & Nussinov, R. (2014). A unified view of “how allostery works”. PLoS Computational Biology, 10, e1003394. doi:10.1371/journal.pcbi.1003394
  • Vasilyeva, A., Clodfelter, J. E., Rector, B., Hollis, T., Scarpinato, K. D., & Salsbury, F. R. (2009). Small molecule induction of MSH2-dependent cell death suggests a vital role of mismatch repair proteins in cell death. DNA Repair, 8, 103–113. doi:10.1016/j.dnarep.2008.09.008
  • Veltman, O. R., Vriend, G., Middelhoven, P. J., van den Burg, B., Venema, G., & Eijsink, V. G. (1996). Analysis of structural determinants of the stability of thermolysinlike proteases by molecular modelling and site-directed mutagenesis. Protein Engineering, 9, 1181–1189.10.1093/protein/9.12.1181
  • Veltman, O. R., Vriend, G., Hardy, F., Mansfeld, J., van den Burg, B., Venema, G., & Eijsink, V. G. (1997). Mutational analysis of a surface area that is critical for the thermal stability of thermolysin-like proteases. European Journal of Biochemistry, 248, 433–440.10.1111/ejb.1997.248.issue-2
  • Verhamme, I. M., Olson, S. T., Tollefsen, D. M., & Bock, P. E. (2002). Binding of exosite ligands to human thrombin: Re-evaluation of allosteric linkage between thrombin exosites I and II. Journal of Biological Chemistry, 277, 6788–6798. doi:10.1074/jbc.M110257200
  • WHO | Estimates for 2000–2012. (n.d.). Retrieved November 29, 2015, from http://www.who.int/healthinfo/global_burden_disease/estimates/en/index1.html
  • World Health Organization. (2014). WHO methods and data sources for country – Level causes of death. Retrieved from http://www.who.int/healthinfo/statistics/GlobalCOD_method.pdf
  • Xiao, J., & Salsbury, F. R. (2016). A Matlab script to perform PCA on molecular dynamics trajectories. Figshare. doi:10.6084/m9.figshare.3842877.v3
  • Yuan, Y., Knaggs, M. H., Poole, L. B., Fetrow, J. S., & Salsbury, F. R. (2010). Conformational and oligomeric effects on the cysteine pK a of tryparedoxin peroxidase. Journal of Biomolecular Structure & Dynamics, 28, 51–70. doi:10.1080/07391102.2010.10507343
  • Zhou, G., Huang, X., & Qu, Y. (2010). The binding effect of aptamers on thrombin. Biochemical Engineering Journal, 52, 117–122. doi:10.1016/j.bej.2010.07.007

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.