Functional roles of magnesium binding to extracellular signal-regulated kinase 2 explored by molecular dynamics simulations and principal component analysis

References

• Aronov, A. M. , Baker, C. , Bemis, G. W. , Cao, J. , Chen, G. , Ford, P. J. , … Jacobs, M. (2007). Flipped out: Structure-guided design of selective pyrazolylpyrrole ERK inhibitors. Journal of Medicinal Chemistry , 50 , 1280–1287.10.1021/jm061381f
   PubMed Web of Science ®Google Scholar
• Case, D. A. , Darden, T. A. , Cheatham III, T. E. , Simmerling, C. L. , Wang, J. , Duke, R. E. , … Kollman, P. A. (2012). AMBER 12 . San Francisco: University of California.
   Google Scholar
• Cedeño, S. , Cifarelli, D. F. , Blasini, A. M. , Paris, M. , Placeres, F. , Alonso, G. , & Rodriguez, M. A. (2003). Defective activity of ERK-1 and ERK-2 mitogen-activated protein kinases in peripheral blood T lymphocytes from patients with systemic lupus erythematosus: potential role of altered coupling of Ras guanine nucleotide exchange factor hSos to adapter protein Grb2 in lupus T cells. Clinical Immunology , 106 , 41–49.10.1016/S1521-6616(02)00052-9
   PubMed Web of Science ®Google Scholar
• Chen, J. (2016). Drug resistance mechanisms of three mutations V32I, I47 V and V82I in HIV-1 protease toward inhibitors probed by molecular dynamics simulations and binding free energy predictions. RSC Advances , 6 , 58573–58585.10.1039/C6RA09201B
   Web of Science ®Google Scholar
• Chen, Y. , He, Y.-J. , Wu, M. , Yan, G. , Li, Y. , Zhang, J. , & Chen, H.-F. (2010). Insight into the stability of cross-β amyloid fibril from molecular dynamics simulation. Biopolymers , 93 , 578–586.
   PubMed Web of Science ®Google Scholar
• Chen, J. , Wang, J. , Zhang, Q. , Chen, K. , & Zhu, W. (2015a). A comparative study of trypsin specificity based on QM/MM molecular dynamics simulation and QM/MM GBSA calculation. Journal of Biomolecular Structure and Dynamics , 33 , 2606–2618.10.1080/07391102.2014.1003146
   PubMed Web of Science ®Google Scholar
• Chen, J. , Wang, J. , Zhang, Q. , Chen, K. , & Zhu, W. (2015b). Probing origin of binding difference of inhibitors to MDM2 and MDMX by polarizable molecular dynamics simulation and QM/MM-GBSA calculation. Scientific Reports , 5 , 17421.10.1038/srep17421
   PubMed Web of Science ®Google Scholar
• Chen, J. , Wang, X. , Zhu, T. , Zhang, Q. , & Zhang, J. Z. H. (2015). A comparative insight into amprenavir resistance of mutations V32I, G48 V, I50 V, I54 V, and I84 V in HIV-1 protease based on thermodynamic integration and MM-PBSA methods. Journal of Chemical Information Modeling , 55 , 1903–1913.10.1021/acs.jcim.5b00173
   PubMed Web of Science ®Google Scholar
• Cohen, P. (2002). Protein kinases–the major drug targets of the twenty-first century? Nature Reviews Drug Discovery , 1 , 309–315.10.1038/nrd773
   PubMed Web of Science ®Google Scholar
• 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 , 10089–10092.10.1063/1.464397
   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. The Journal of Chemical Physics , 103 , 8577–8593.10.1063/1.470117
   Web of Science ®Google Scholar
• Eunan Hendron, J. D. S. (2002). Activation of mitogen-activated protein kinase (mitogen-activated protein kinase/extracellular signal-regulated kinase) cascade by aldosterone. Molecular Biology of the Cell , 13 , 3042–3054.10.1091/mbc.E02-05-0260
   PubMed Web of Science ®Google Scholar
• Fox, J. M. , Kang, K. , Sherman, W. , Héroux, A. , Sastry, G. M. , Baghbanzadeh, M. , … Whitesides, G. M. (2015). Interactions between Hofmeister anions and the binding pocket of a protein. Journal of the American Chemical Society , 137 , 3859–3866.10.1021/jacs.5b00187
   PubMed Web of Science ®Google Scholar
• Gaestel, M. , Kotlyarov, A. , & Kracht, M. (2009). Targeting innate immunity protein kinase signalling in inflammation. Nature Reviews Drug Discovery , 8 , 480–499.10.1038/nrd2829
   PubMed Web of Science ®Google Scholar
• García, A. E. (1992). Large-amplitude nonlinear motions in proteins. Physical Review Letters , 68 , 2696–2699.10.1103/PhysRevLett.68.2696
   PubMed Web of Science ®Google Scholar
• Gohlke, H. , Kiel, C. , & Case, D. A. (2003). Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras–RalGDS complexes. Journal of Molecular Biology , 330 , 891–913.10.1016/S0022-2836(03)00610-7
   PubMed Web of Science ®Google Scholar
• Hu, G. , Cao, Z. , Xu, S. , Wang, W. , & Wang, J. (2015). Revealing the binding modes and the unbinding of 14-3-3σ proteins and inhibitors by computational methods. Scientific Reports , 5 , 16481.10.1038/srep16481
   PubMed Web of Science ®Google Scholar
• Hu, G. , Ma, A. , Dou, X. , Zhao, L. , & Wang, J. (2016). Computational studies of a mechanism for binding and drug resistance in the wild type and four mutations of HIV-1 protease with a GRL-0519 inhibitor. International Journal of Molecular Sciences , 17 , 819.10.3390/ijms17060819
   Web of Science ®Google Scholar
• Huang, W. , Cai, L. , Chen, C. , Xie, X. , Zhao, Q. , Zhao, X. , … Peng, C. (2016). Computational analysis of spiro-oxindole inhibitors of the MDM2-p53 interaction: insights and selection of novel inhibitors. Journal of Biomolecular Structure and Dynamics , 34 , 341–351.10.1080/07391102.2015.1031178
   PubMed Web of Science ®Google Scholar
• Ichiye, T. , & Karplus, M. (1991). Collective motions in proteins: A covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations. Proteins: Structure, Function, and Genetics , 11 , 205–217.10.1002/(ISSN)1097-0134
   PubMed Web of Science ®Google Scholar
• Izaguirre, J. A. , Catarello, D. P. , Wozniak, J. M. , & Skeel, R. D. (2001). Langevin stabilization of molecular dynamics. The Journal of Chemical Physics , 114 , 2090–2098.10.1063/1.1332996
   Web of Science ®Google Scholar
• Jia, X. , Wang, M. , Shao, Y. , König, G. , Brooks, B. R. , Zhang, J. Z. , & Mei, Y. (2016). Calculations of solvation free energy through energy reweighting from molecular mechanics to quantum mechanics. Journal of Chemical Theory & Computation , 12 , 499–511.10.1021/acs.jctc.5b00920
   PubMed Web of Science ®Google Scholar
• Jiang, Y. , Zhang, H. , & Tan, T. (2016). Rational design of methodology-independent metal parameters using a nonbonded dummy model. Journal of Chemical Theory & Computation , 12 , 3250–3260.10.1021/acs.jctc.6b00223
   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. The Journal of Chemical Physics , 79 , 926–935.10.1063/1.445869
   Web of Science ®Google Scholar
• Kamps, M. P. , Taylor, S. S. , & Sefton, B. M. (1983). Direct evidence that oncogenic tyrosine kinases and cyclic AMP-dependent protein kinase have homologous ATP-binding sites. Nature , 310 , 589–592.
   Web of Science ®Google Scholar
• Laberge, M. , & Yonetani, T. (2008). Molecular dynamics simulations of hemoglobin A in different states and bound to DPG: Effector-linked perturbation of tertiary conformations and HbA concerted dynamics. Biophysical Journal , 94 , 2737–2751.10.1529/biophysj.107.114942
   PubMed Web of Science ®Google Scholar
• 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 , 1099–1112.10.1002/(ISSN)1097-0282
   PubMed Web of Science ®Google Scholar
• Li, G. , Shen, H. , Zhang, D. , Yan, L. , & Wang, H. (2015). Coarse-grained modeling of nucleic acids using anisotropic gay-berne and electric multipole potentials. Journal of Chemical Theory & Computation , 12 , 676–693.
   Web of Science ®Google Scholar
• Lu, S.-Y. , Huang, Z.-M. , Huang, W.-K. , Liu, X.-Y. , Chen, Y.-Y. , Shi, T. , & Zhang, J. (2013). How calcium inhibits the magnesium-dependent kinase gsk3β: A molecular simulation study. Proteins: Structure, Function, and Bioinformatics , 81 , 740–753.10.1002/prot.v81.5
   PubMed Web of Science ®Google Scholar
• 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 , e1003831.10.1371/journal.pcbi.1003831
   PubMed Web of Science ®Google Scholar
• 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 , 1725–1734.10.1016/j.str.2015.06.027
   PubMed Web of Science ®Google Scholar
• Lusetti, S. L. , Shaw, J. J. , & Cox, M. M. (2003). Magnesium ion-dependent activation of the RecA protein involves the C terminus. Journal of Biological Chemistry , 278 , 16381–16388.10.1074/jbc.M212916200
   PubMed Web of Science ®Google Scholar
• Maier, J. A. , Martinez, C. , Kasavajhala, K. , Wickstrom, L. , Hauser, K. E. , & Simmerling, C. (2015). ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB. Journal of Chemical Theory and Computation , 11 , 3696–3713.10.1021/acs.jctc.5b00255
   PubMed Web of Science ®Google Scholar
• McLachlan, A. D. (1979). Gene duplications in the structural evolution of chymotrypsin. Journal of Molecular Biology , 128 , 49–79.10.1016/0022-2836(79)90308-5
   PubMed Web of Science ®Google Scholar
• Meagher, K. L. , Redman, L. T. , & Carlson, H. A. (2003). Development of polyphosphate parameters for use with the AMBER force field. Journal of Computational Chemistry , 24 , 1016–1025.10.1002/jcc.v24:9
   PubMed Web of Science ®Google Scholar
• Oelschlaeger, P. , Klahn, M. , Beard, W. A. , Wilson, S. H. , & Warshel, A. (2007). Magnesium-cationic dummy atom molecules enhance representation of DNA polymerase β in molecular dynamics simulations: Improved accuracy in studies of structural features and mutational effects. Journal of Molecular Biology , 366 , 687–701.10.1016/j.jmb.2006.10.095
   PubMed Web of Science ®Google Scholar
• Onufriev, A. , Bashford, D. , & Case, D. A. (2004). Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins: Structure, Function, and Bioinformatics , 55 , 383–394.10.1002/prot.20033
   PubMed Web of Science ®Google Scholar
• Peeraer, Y. , Rabijns, A. , Collet, J. F. , Van Schaftingen, E. , & De Ranter, C. (2004). How calcium inhibits the magnesium-dependent enzyme human phosphoserine phosphatase. European Journal of Biochemistry , 271 , 3421–3427.10.1111/ejb.2004.271.issue-16
   PubMedGoogle Scholar
• Perry, G. , Roder, H. , Nunomura, A. , Takeda, A. , Friedlich, A. L. , Zhu, X. , … Smith, M. A. (1999). Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. NeuroReport , 10 , 2411–2415.10.1097/00001756-199908020-00035
   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 , 3084–3095.10.1021/ct400341p
   PubMed Web of Science ®Google Scholar
• Ryckaert, J.-P. , Ciccotti, G. , & Berendsen, H. J. C. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. Journal of Computational Physics , 23 , 327–341.10.1016/0021-9991(77)90098-5
   Web of Science ®Google Scholar
• Satoh, Y. , Kobayashi, Y. , Takeuchi, A. , Pages, G. , Pouyssegur, J. , & Kazama, T. (2011). Deletion of ERK1 and ERK2 in the CNS causes cortical abnormalities and neonatal lethality: Erk1 Deficiency enhances the impairment of neurogenesis in Erk2-deficient mice. Journal of Neuroscience , 31 , 1149–1155.10.1523/JNEUROSCI.2243-10.2011
   PubMed Web of Science ®Google Scholar
• Seger, R. , Ahn, N. G. , Boulton, T. G. , Yancopoulos, G. D. , Panayotatos, N. , Radziejewska, E. , … Krebs, E. G. (1991). Microtubule-associated protein 2 kinases, ERK1 and ERK2, undergo autophosphorylation on both tyrosine and threonine residues: Implications for their mechanism of activation. Proceedings of the National Academy of Sciences , 88 , 6142–6146.10.1073/pnas.88.14.6142
   PubMed Web of Science ®Google Scholar
• Turjanski, A. G. , Hummer, G. , & Gutkind, J. S. (2009). How mitogen-activated protein kinases recognize and phosphorylate their targets: A QM/MM study. Journal of the American Chemical Society , 131 , 6141–6148.10.1021/ja8071995
   PubMed Web of Science ®Google Scholar
• Waas, W. F. , & Dalby, K. N. (2003). Physiological concentrations of divalent magnesium ion activate the serine/threonine specific protein kinase ERK2. Biochemistry , 42 , 2960–2970.10.1021/bi027171w
   PubMed Web of Science ®Google Scholar
• Wang, W. , & Kollman, P. A. (2001). Computational study of protein specificity: The molecular basis of HIV-1 protease drug resistance. Proceedings of the National Academy of Sciences , 98 , 14937–14942.10.1073/pnas.251265598
   PubMed Web of Science ®Google Scholar
• Wang, J. , Morin, P. , Wang, W. , & Kollman, P. A. (2001). Use of MM-PBSA in reproducing the binding free energies to HIV-1 RT of TIBO derivatives and predicting the binding mode to HIV-1 RT of efavirenz by docking and MM-PBSA. Journal of the American Chemical Society , 123 , 5221–5230.10.1021/ja003834q
   PubMed Web of Science ®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 , 1157–1174.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Wang, J. , Shao, Q. , Cossins, B. P. , Shi, J. , Chen, K. , & Zhu, W. (2016). Thermodynamics calculation of protein–ligand interactions by QM/MM polarizable charge parameters. Journal of Biomolecular Structure and Dynamics , 34 , 163–176.10.1080/07391102.2015.1019928
   PubMed Web of Science ®Google Scholar
• Ward, R. A. , Colclough, N. , Challinor, M. , Debreczeni, J. E. , Eckersley, K. , Fairley, G. , … Greenwood, R. (2015). Structure-guided design of highly selective and potent covalent inhibitors of ERK1/2. Journal of Medicinal Chemistry , 58 , 4790–4801.10.1021/acs.jmedchem.5b00466
   PubMed Web of Science ®Google Scholar
• Wu, R. , Hu, P. , Wang, S. , Cao, Z. , & Zhang, Y. (2009). Flexibility of catalytic zinc coordination in thermolysin and HDAC8: A Born−Oppenheimer ab initio QM/MM molecular dynamics study. Journal of Chemical Theory & Computation , 6 , 337–343.
   PubMed Web of Science ®Google Scholar
• Wu, E. L. , Wong, K.-Y. , Zhang, X. , Han, K. , & Gao, J. (2009). Determination of the structure form of the fourth ligand of zinc in acutolysin a using combined quantum mechanical and molecular mechanical simulation. The Journal of Physical Chemistry B , 113 , 2477–2485.10.1021/jp808182y
   PubMed Web of Science ®Google Scholar
• Yang, M. , Zhang, X. , & Han, K. (2010). Molecular dynamics simulation of SRP GTPases: Towards an understanding of the complex formation from equilibrium fluctuations. Proteins: Structure, Function, and Bioinformatics , 78 , 2222–2237.10.1002/prot.v78:10
   PubMed Web of Science ®Google Scholar
• Yang, M.-J. , Pang, X.-Q. , Zhang, X. , & Han, K.-L. (2011). Molecular dynamics simulation reveals preorganization of the chloroplast FtsY towards complex formation induced by GTP binding. Journal of Structural Biology , 173 , 57–66.10.1016/j.jsb.2010.07.013
   PubMed Web of Science ®Google Scholar
• Zhang, J. , Shapiro, P. , & Pozharski, E. (2012). Structure of extracellular signal-regulated kinase 2 in complex with ATP and ADP. Acta Crystallographica , 68 , 1434–1439.
   Google Scholar
• Zheng, C. F. , & Guan, K. L. (1993). Properties of MEKs, the kinases that phosphorylate and activate the extracellular signal-regulated kinases. Journal of Biological Chemistry , 268 , 23933–23939.
   PubMed Web of Science ®Google Scholar
• Zhu, T. , Xiao, X. , Ji, C. , & Zhang, J. Z. H. (2013). A new quantum calibrated force field for zinc-protein complex. Journal of Chemical Theory and Computation , 9 , 1788–1798.10.1021/ct301091z
   PubMed Web of Science ®Google Scholar
• Zurita, A. , Zhang, Y. , Pedersen, L. , Darden, T. , & Birnbaumer, L. (2010). Obligatory role in GTP hydrolysis for the amide carbonyl oxygen of the Mg2+-coordinating Thr of regulatory GTPases. Proceedings of the National Academy of Sciences , 107 , 9596–9601.10.1073/pnas.1004803107
   PubMed Web of Science ®Google Scholar