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Research Article

Molecular dynamics simulations provide insights into the origin of gleevec’s selectivity toward human tyrosine kinases

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Pages 2733-2744 | Received 20 Mar 2018, Accepted 15 May 2018, Published online: 01 Nov 2018

References

  • Agafonov, R. V., Wilson, C., Otten, R., Buosi, V., & Kern, D. (2014). Energetic dissection of Gleevec's selectivity toward human tyrosine kinases. Nature Structural & Molecular Biology, 21(10), 848–853.
  • Aleksandrov, A., & Simonson, T. (2010). Molecular dynamics simulations show that conformational selection governs the binding preferences of imatinib for several tyrosine kinases. Journal of Biological Chemistry, 285(18), 13807–13815.
  • Azam, M., Nardi, V., Shakespeare, W. C., Metcalf, C. A., Bohacek, R. S., Wang, Y., … Bornmann, W. G. (2006). Activity of dual SRC-ABL inhibitors highlights the role of BCR/ABL kinase dynamics in drug resistance. Proceedings of the National Academy of Sciences, 103(24), 9244–9249.
  • Capdeville, R., Buchdunger, E., Zimmermann, J., & Matter, A. (2002). Glivec (STI571, imatinib), a rationally developed, targeted anticancer drug. Nature Reviews Drug Discovery, 1(7), 493–502.
  • Case, D., Darden, T., Cheatham, T., III, Simmerling, C., Wang, J., Duke, R., … Merz, K. (2012). AMBER 12. San Francisco: University of California.
  • Chatterjee, A., & Datta, P. P. (2017). Intrisinc GTPase activity of a ribosomal maturation protein CgtA is assocaited with its inter-domain movement: Insights into from MD simulations and biochemical studies. Journal of Biomolecular Structure and Dynamics, 35(12), 2578–2587.
  • Chen, F., Liu, H., Sun, H., Pan, P., Li, Y., Li, D., & Hou, T. (2016). Assessing the performance of the MM/PBSA and MM/GBSA methods. 6. Capability to predict protein-protein binding free energies and re-rank binding poses generated by protein-protein docking. Physical Chemistry Chemical Physics, 18(32), 22129–22139.
  • Cowan-Jacob, S. W., Fendrich, G., Manley, P. W., Jahnke, W., Fabbro, D., Liebetanz, J., & Meyer, T. (2005). The crystal structure of a c-Src complex in an active conformation suggests possible steps in c-Src activation. Structure, 13(6), 861–871.
  • Dar, A. C., Lopez, M. S., & Shokat, K. M. (2008). Small molecule recognition of c-Src via the Imatinib-binding conformation. Chemistry & Biology, 15(10), 1015–1022.
  • 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(12), 10089–10092.
  • Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., … Kollman, P. (2003). A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. Journal of Computational Chemistry, 24(16), 1999–2012.
  • Fiser, A., & Sali, A. (2003). Modeller: Generation and refinement of homology-based protein structure models. Methods in Enzymology, 374, 461–491.
  • Frisch, M., Trucks, G., Schlegel, H., Scuseria, G., Robb, M., Cheeseman, J. Parr. (2009). Gaussian 09, revision A. 02. Wallingford, CT: Gaussian, Inc.
  • Glykos, N. M. (2006). Software news and updates carma: A molecular dynamics analysis program. Journal of Computational Chemistry, 27(14), 1765–1768.
  • Guimaraes, C. R., Rai, B. K., Munchhof, M. J., Liu, S., Wang, J., Bhattacharya, S. K., & Buckbinder, L. (2011). Understanding the impact of the P-loop conformation on kinase selectivity. Journal of Chemical Information and Modeling, 51(6), 1199–1204.
  • Hertig, S., Latorraca, N. R., & Dror, R. O. (2016). Revealing atomic-level mechanisms of protein allostery with molecular dynamics simulations. PLoS Computational Biology, 12(6), e1004746.
  • Hou, T., Li, N., Li, Y., & Wang, W. (2012). Characterization of domain-peptide interaction interface: Prediction of SH3 domain-mediated protein-protein interaction network in yeast by generic structure-based models. Journal of Proteome Research, 11(5), 2982–2995.
  • Hou, T., Wang, J., Li, Y., & Wang, W. (2011). Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. Journal of Chemical Information and Modeling, 51(1), 69–82.
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38.
  • Huse, M., & Kuriyan, J. (2002). The conformational plasticity of protein kinases. Cell, 109(3), 275–282.
  • 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, 79(2), 926–935.
  • Levinson, N. M., Kuchment, O., Shen, K., Young, M. A., Koldobskiy, M., Karplus, M., … Kuriyan, J. (2006). A Src-like inactive conformation in the abl tyrosine kinase domain. PLoS Biology, 4(5), e144
  • Levitzki, A. (2003). Protein kinase inhibitors as a therapeutic modality. Accounts of Chemical Research, 36(6), 462–469.
  • Lin, Y. L., Meng, Y., Jiang, W., & Roux, B. (2013). Explaining why Gleevec is a specific and potent inhibitor of Abl kinase. Proceedings of the National Academy of Sciences of the United States of America, 110(5), 1664–1669.
  • Lovera, S., Sutto, L., Boubeva, R., Scapozza, L., Dolker, N., & Gervasio, F. L. (2012). The different flexibility of c-Src and c-Abl kinases regulates the accessibility of a druggable inactive conformation. Journal of the American Chemical Society, 134(5), 2496–2499.
  • Lu, S., Deng, R., Jiang, H., Song, H., Li, S., Shen, Q., … Zhang, J. (2015). The Mechanism of ATP-dependent allosteric protection of Akt kinase phosphorylation. Structure, 23(9), 1725–1734.
  • Lu, S., Huang, W., Wang, Q., Shen, Q., Li, S., Nussinov, R., & Zhang, J. (2014). The structural basis of ATP as an allosteric modulator. PLoS Computational Biology, 10(9), e1003831
  • Lu, S., Jang, H., Gu, S., Zhang, J., & Nussinov, R. (2016a). Drugging Ras GTPase: A comprehensive mechanistic and signaling structural view. Chemical Society Reviews, 45(18), 4929–4952.
  • Lu, S., Jang, H., Muratcioglu, S., Gursoy, A., Keskin, O., Nussinov, R., & Zhang, J. (2016b). Ras conformational ensembles, allostery, and signaling. Chemical Reviews, 116(11), 6607–6665.
  • Lu, S., Ji, M., Ni, D., & Zhang, J. (2018). Discovery of hidden allosteric sites as novel targets for allosteric drug design. Drug Discovery Today, 23(2), 359–365.
  • Lu, S., Li, S., & Zhang, J. (2014). Harnessing allostery: A novel approach to drug discovery. Med Res Rev, 34(6), 1242–1285.
  • Lu, S., & Zhang, J. (2017). Designed covalent allosteric modulators: An emerging paradigm in drug discovery. Drug Discovery Today, 22(2), 447–453.
  • Manning, G., Whyte, D. B., Martinez, R., Hunter, T., & Sudarsanam, S. (2002). The protein kinase complement of the human genome. Science, 298(5600), 1912–1934.
  • Matthews, D. J., & Gerritsen, M. E. (2011). Targeting protein kinases for cancer therapy, John Wiley & Sons.ISBN 978-1-118-21077-2.
  • Mou, L., Cui, T., Liu, W., Zhang, H., Cai, Z., Lu, S., & Gao, G. (2017). Microsecond molecualr dynamics simulations provide insight into the ATP-competitive inhibitor-induced allosteric protection of Akt kinase phorphoeylation. Chemical Biology & Drug Design, 89(5), 723–731.
  • Nagar, B., Bornmann, W. G., Pellicena, P., Schindler, T., Veach, D. R., Miller, W. T., … Kuriyan, J. (2002). Crystal structures of the kinase domain of c-Abl in complex with the small molecule inhibitors PD173955 and imatinib (STI-571. ). Cancer Research, 62, 4236–4243.
  • Nagar, B., Hantschel, O., Young, M. A., Scheffzek, K., Veach, D., Bornmann, W., … Kuriyan, J. (2003). Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell, 112(6), 859–871.
  • Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341.
  • Sanjeev, A., Sahu, R. K., & Mattaparthi, V. S. K. (2017). Potential of mean force and molecular dynamics study on the transient interactions between α and β synuclein that drive inhibition of α-synuclein aggregation. Journal of Biomolecular Structure and Dynamics, 35(15), 3342–3353.
  • Saraste, M., Sibbald, P. R., & Wittinghofer, A. (1990). The P-loop-a common motif in ATP- and GTP-binding proteins. Trends in Biochemical Sciences, 15(11), 430–434.
  • Schindler, T., Bornmann, W., Pellicena, P., Miller, W. T., Clarkson, B., & Kuriyan, J. (2000). Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science, 289(5486), 1938–1942.
  • Sciabola, S., Stanton, R. V., Wittkopp, S., Wildman, S., Moshinsky, D., Potluri, S., & Xi, H. (2008). Predicting kinase selectivity profiles using Free-Wilson QSAR analysis. Journal of Chemical Information and Modeling, 48(9), 1851–1867.
  • Seeliger, M. A., Nagar, B., Frank, F., Cao, X., Henderson, M. N., & Kuriyan, J. (2007). c-Src binds to the cancer drug imatinib with an inactive Abl/c-Kit conformation and a distributed thermodynamic penalty. Structure, 15(3), 299–311.
  • Sun, H., Li, Y., Shen, M., Tian, S., Xu, L., Pan, P., … Hou, T. (2014). Assessing the performance of MM/PBSA and MM/GBSA methods. 5. Improved docking performance using high solute dielectric constant MM/GBSA and MM/PBSA rescoring. Physical Chemistry Chemical Physics, 16(40), 22035–22045.
  • Sun, H., Li, Y., Tian, S., Xu, L., & Hou, T. (2014). Assessing the performance of MM/PBSA and MM/GBSA methods. 4. Accuracies of MM/PBSA and MM/GBSA methodologies evaluated by various simulation protocols using PDBbind data set. Physical Chemistry Chemical Physics, 16(31), 16719–16729.
  • 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.
  • Wang, Y., Zhu, G.-F., Ren, S.-Y., Han, Y.-G., Luo, Y., & Du, L.-F. (2013). Insight into the structural stability of wild type and mutants of the tobacco etch virus protease with molecular dynamics simulations. Journal of Molecular Modeling, 19, 4865–4875.
  • Wenqing, W., Harrison, S. C., & Eck, M. J. (1997). Three-dimensional structure of the tyrosine kinase c-Src. Nature, 385(6617), 595–602.
  • Williams, J. C., Weijland, A., Gonfloni, S., Thompson, A., Courtneidge, S. A., Superti-Furga, G., & Wierenga, R. K. (1997). The 2.35 Å crystal structure of the inactivated form of chicken Src: A dynamic molecule with multiple regulatory interactions. Journal of Molecular Biology, 274(5), 757–775.
  • Wilson, C., Agafonov, R. V., Hoemberger, M., Kutter, S., Zorba, A., Halpin, J., … Kern, D. (2015). Kinase dynamics. Using ancient protein kinases to unravel a modern cancer drug's mechanism. Science, 347(6224), 882–886.
  • Winter, G. E., Rix, U., Carlson, S. M., Gleixner, K. V., Grebien, F., Gridling, M., … Colinge, J. (2012). Systems-pharmacology dissection of a drug synergy in imatinib-resistant CML. Nature Chemical Biology, 8(11), 905–912.
  • Wu, X., & Brooks, B. R. (2003). Self-guided Langevin dynamics simulation method. Chemical Physics Letters, 381(3-4), 512–518.
  • Xu, W., Doshi, A., Lei, M., Eck, M. J., & Harrison, S. C. (1999). Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Molecular Cell, 3(5), 629–638.
  • Xu, L., Sun, H., Li, Y., Wang, J., & Hou, T. (2013). Assessing the performance of MM/PBSA and MM/GBSA methods. 3. The impact of force fields and ligand charge models. The Journal of Physical Chemistry. B, 117(28), 8408–8421.
  • Yang, Y., Shen, Y., Liu, H., & Yao, X. (2011). Molecular dynamics simulation and free energy calculation studies of the binding mechanism of allosteric inhibitors with p38α MAP kinase. Journal of Chemical Information and Modeling, 51(12), 3235–3246.
  • Zhu, J., Li, X., Zhang, S., Ye, H., Zhao, H., Jin, H., & Han, W. (2017). Exploring stereochemical specificity of phosphotriesterase by MM-PBSA and MM-GBSA calculation and steered molecular dynamics simulations. Journal of Biomolecular Structure and Dynamics, 35(14), 3140–3151.

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