First principles calculations of thermodynamics and kinetic parameters and molecular dynamics simulations of acetylcholinesterase reactivators: Can mouse data provide new insights into humans?

Journal of Biomolecular Structure and Dynamics

Volumn 30, Issue 5, 2012, Pages 546-558

  Matos, Karina S ^a   Da Cunha, Elaine F F ^a   Da Silva Gonçalves, Arlan ^b   Wilter, Alan ^c   Kuča, Kamil ^d,e   França, Tanos C C ^f   Ramalho, Teodorico C ^a  

^a FEDERAL UNIVERSITY OF LAVRAS   (Brazil)

^b Federal Institute of Education Science and Technology   (Brazil)

^c EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^d UNIVERSITY OF DEFENCE   (Czech Republic)

^e UNIVERSITY HOSPITAL HRADEC KRALOVE   (Czech Republic)

^f MILITARY INSTITUTE OF ENGINEERING   (Brazil)

Author keywords

Acetylcholinesterase; Chemical mechanism of reactivation; Neurotoxic agents; QM MM

Indexed keywords

ACETYLCHOLINESTERASE; CHOLINESTERASE REACTIVATOR;

ARTICLE; BINDING SITE; CALCULATION; CRYSTALLOGRAPHY; ENZYME KINETICS; ENZYME REACTIVATION; HUMAN; HUMAN VERSUS NONHUMAN DATA; IN VITRO STUDY; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTUM MECHANICS; SEQUENCE ALIGNMENT; THEORETICAL MODEL; THERMODYNAMICS;

ACETYLCHOLINESTERASE; AMINO ACID SEQUENCE; ANIMALS; CHOLINESTERASE INHIBITORS; CHOLINESTERASE REACTIVATORS; HUMANS; KINETICS; MICE; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; OXIMES; SEQUENCE ALIGNMENT; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

MUS MUSCULUS;

EID: 84865637226     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2012.687521     Document Type: Article

References (76)

1. Akten, E.D., Cansu, S., & Doruker, P. (2009). A docking study using atomistic conformersgenerated via elastic network model for cyclosporin a/cyclophilin a complex. Journal of Biomolecular Structure & Dynamics, 27, 13-25.
2. Andrianov, A.M. (2009). Immunophilins and HIV-1 V3 loop for structure-based anti-AIDS drug design. Journal of Biomolecular Structure & Dynamics, 26, 445-454.
3. Ashani, Y., Radic, Z., Tsigelny, I., Vellom, D.C., Pickering, N. A., Quinn, D.M., Taylor, P. (1995). Amino acid residues controlling reactivation of organophosphonyl conjugates of acetylcholinesterase by mono- and bisquaternary oximes. Journal of Biological Chemistry, 11, 6370-6380.
4. Bairagya, H.R., Mukhopadhyay, B.P., & Sekar, K. (2009). An insight to the dynamics of conserved water molecular triad in IMPDH II (Human): Recognition of cofactor and substrate to catalytic Arg 322. Journal of Biomolecular Structure & Dynamics, 27, 149-158.
5. Barnard, E.A. (1974). Neuromuscular transmission - enzymatic destruction of acetylcholine. In J.I. Hubbard (Ed.), The peripheral nervous system (pp. 30-50). New York, NY: Plenum Press.
6. Bernard, P.P., Kireev, D.B., Pintore, M., Chrétien, J.R., Fortier, P.L., & Froment, D. (2000). A CoMFA study of enantiomeric organophosphorus inhibitors of acetylcholinesteras. Journal of Molecular Modeling, 6, 618-629.
7. Black, R.M., & Harrison, J.M. (1996). The chemistry of organophosphorus chemical warfare agents. In F.R. Hartley (Ed.), The chemistry of organophosphorus compounds (Vol. 4, pp. 120-240). Chichester: Wiley.
8. Borkar, A., Ghosh, I., & Bhattacharyya, D. (2010). Structure and dynamics of double helical DNA in torsion angle hyperspace: A molecular mechanics approach. Journal of Biomolecular Structure & Dynamics, 27, 695-712.
9. Brooks, B.R., Brooks C.L. III, MacKerell Jr., A.D., Nilsson, L., Petrella, R.J., Roux, B. Brunger, A.T. (2007). Version 1.2 of the crystallography and NMR system. Nature Protocols, 2, 2728-2733.
10. Cambria, M.T., Di Marino, D., Falconi, M., Garavaglia, S., & Cambria, A. (2010). Dockingsimulation and competitive experiments validate the interaction between the 2,5- xylidine Inhibitor and Rigidoporus lignosus laccase. Journal of Biomolecular Structure & Dynamics, 27, 501-509.
11. Chen, C.Y.C. (2009). Weighted equation and rules - a novel concept for evaluating protein-ligand interaction. Journal of Biomolecular Structure & Dynamics, 27, 271-282.
12. Chen, C.Y. (2010). Virtual screening and drug design for PdDe-5 receptor from traditional Chinese medicine database. Journal of Biomolecular Structure & Dynamics, 27, 627-640.
13. Chen, C.Y., Chang, Y.H., Bau, D.T., Huang, H.J., Tsai, F.J., Tsai, C.H., & Chen, C.Y.C. (2009). Ligand-based dual target drug design for H1N1: Swine flu - a preliminary first study. Journal of Biomolecular Structure & Dynamics, 27, 171-178.
14. Cordomi, A., & Perez, J.J. (2009). Structural rearrangements of rhodopsin subunits in a dimer complex: A molecular dynamics simulation study. Journal of Biomolecular Structure & Dynamics, 27, 127-147.
15. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K. M., Ferguson, D.M., Kollman, P.A. (1995). A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. Journal of the American Chemical Society, 117, 5179-5197.
16. da Cunha, E.F.F., Barbosa, E.F., Oliveira, A.A., & Ramalho, T. C. (2010). Molecular modeling of mycobacterium tuberculosis DNA gyrase and its molecular docking study with gatifloxacin inhibitors. Journal of Biomolecular Structure & Dynamics, 27, 619-625.
17. da Cunha, E.F.F., Ramalho, T.C., Mancini, D.T., Fonseca, E. M.B., & Oliveira, A.A. (2010). New approaches to the development of anti-protozoan drug candidates: A review of patents. Journal of the Brazilian Chemical Society, 21, 1787-1806.
18. Dvir, H., Silman, I., Harel, M., Rosenberry, T.L., & Sussman, J.L. (2010). Acetylcholinesterase: From 3D structure to function. Chemico-Biological Interactions, 187, 10-22.
19. Ekström, F.J., Astot, C., & Pang, Y.P. (2007). Novel nerveagent antidote design based on crystallographic and mass spectrometric analyses of tabun-conjugated acetylcholinesterase in complex with antidotes. Clinical Pharmacology and Therapeutics, 82(3), 282-293.
20. Ekström, F., Hörnberg, A., Artursson, E., Hammarström, L., Schneider, G., & Pang, Y. (2009). Structure of HI-6NSarin- Acetylcholinesterase determined by X-ray crystallography and molecular dynamics simulation: Reactivator mechanism and design. PLoS ONE, 4, e5957.
21. Ekström, F.J., Yuan-Ping, P., Boman, M., Artursson, E., Akfur, C., & Börjegren, S. (2006). Crystal structures of acetylcholinesterase in complex with HI-6, Ortho-7 and obidoxime: Structural basis for differences in the ability to reactivate tabun conjugates. Biochemical Pharmacology, 72, 597-607.
22. Frisch, M.J., Trucks, G.W., Schlegel, H.B., Scuseria, G.E., Robb, M.A., Cheeseman, J.R., Pople, J.A. (2004). Gaussian, Inc. Wallingford, CT.
23. Gonçalves, A.S., França, T.C.C., Figueroa-Villar, J.D., & Pascutti, P.G. (2010). Conformational analysis of toxogonine, TMB-4 and HI-6 using PM6 and RM1 methods. Journal of the Brazilian Chemical Society, 21, 179-184.
24. Gonçalves, A.S., França, T.C.C., Figueroa-Villar, J.D., & Pascutti, P.G. (2011). Molecular dynamics simulations and QM/MM studies of the reactivation by 2-PAM of tabun inhibited human acethylcolinesterase. Journal of the Brazilian Chemical Society, 22, 155-165.
25. Gonçalves, A.S., França, T.C.C., Wilter, A., & Figueroa-Villar, J.D. (2006). Molecular dynamics of the interaction of pralidoxime and deazapralidoxime with acetylcholinesterase inhibited by the neurotoxic agent tabun. Journal of the Brazilian Chemical Society, 17, 968-975.
26. Guex, N., & Peitsch, M.C. (1997). Peitsch, swiss-model and Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis, 18, 2714.2723.
27. Guimaraes, A.P., Franca, T.C.C., Ramalho, T.C., Renno, M.N., da Cunha, E.F.F., Matos, K.S., Mancini, D.T., & Ku.a, K. (2011). Docking studies and effects of syn-anti isomery ofoximes derived from pyridine imidazol bicycled systems as potential human acetylcholinesterase reactivators. Journal of Applied Biomedicine, 9, 163-171.
28. Hage-Melim, L.I.D., da Silva, C.H.T.D., Semighini, E.P., Taft, C.A., & Sampaio, S.V. (2009). Computer-aided drug design of novel PLA2 inhibitor candidates for treatment of snakebite. Journal of Biomolecular Structure & Dynamics, 27, 27-35.
29. Hehre, W.J., Deppmeier, B.J., & Klunzinger, P.E. (1999). PC SPARTAN Pro. Irvine, CA: Wavefunction.
30. Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4, 435-447.
31. Huang, H.J., Lee, K.J., Yu, H.W., Chen, C.Y., Hsu, C.H., Chen, H.Y., Tsai, F.J., & Chen, C.Y.C. (2010). Structure-based and ligand-based drug design for HER 2 receptor. Journal of Biomolecular Structure & Dynamics, 28, 23-37.
32. Huang, H.J., Lee, K.J., Yu, H.W., Chen, H.Y., Tsai, F.J., & Chen, C.Y. (2010). A novel strategy for designing the selective PPAR agonist by the gsum of activityh model. Journal of Biomolecular Structure & Dynamics, 28, 187-200.
33. Humphrey, W., Dalke, A., & Schulte, K. (1996). VMD. visual molecular dynamics. Journal of Molecular Graphics, 14, 33-38.
34. Jin, B., Lee, H.M., & Kim, S.K. (2010). Conformational analysis of genotoxic benzo[a]pyrene-7,8-dione-duplex DNA adducts using a molecular dynamics method. Journal of Biomolecular Structure & Dynamics, 27, 457-464.
35. Jorgensen, W.L. (1991). Rusting of the lock and key model for protein-ligand binding. Science, 254, 954-955.
36. 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 Computational Physics, 79, 926-935.
37. Jorgensen, W.L., Maxwell, D.S., & Tirado-Rives, J. (1996). Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. Journal of the American Chemical Society, 118(45), 11225-11236.
38. Kahlon, A.K., Roy, S., & Sharma, A. (2010). Molecular docking studies to map the binding site of squalene synthase inhibitors on dehydrosqualene synthase of Staphylococcus aureus. Journal of Biomolecular Structure & Dynamics, 28, 201-210.
39. Kassa, J., Kuca, K., Bartosova, L., & Kunesova, G. (2007). The development of new structural analogues of oximes for the antidotal treatment of poisoning by nerve agents and the comparison of their reactivating and therapeutic efficacy with currently available oximes. Current Organic Chemistry, 11, 267-283.
40. Koradi, R., Billeter, M., & Wuthrich, K. (1996). MOLMOL: A program for display and analysis of macromolecular structures. Journal of Molecular Graphics, 14, 51-55.
41. Koshy, C., Parthiban, M., & Sowdhamini, R. (2010). 100 ns molecular dynamics simulations to study intramolecular conformational changes in bax. Journal of Biomolecular Structure & Dynamics, 28, 71-83.
42. Kryger, G., Harel, M., Giles, K., Toker, L., Velan, B., Lazar, A., c Sussman, J.L. (2000). Structures of recombinant native and E202Q mutant human acetylcholinesterase complexed with the snake-venom toxin fasciculin-II. Acta Crystallographica. Section D, Biological Crystallography, 56, 1385-1394.
43. Likhatskaya, G.N., Solov'eva, T.F., Novikova, O.D., Issaeva, M.P., Gusev, K.V., Kryzhko, I.B., Nurminski, E.A. (2005). Homology models of the Yersinia pseudotuberculosis and Yersinia pestis general porins and comparative analysis of their functional and antigenic regions. Journal of Biomolecular Structure & Dynamics, 23, 113-232.
44. Maseras, F., & Morokuma, K. (1995). IMOMM: A new integrated ab initio + molecular mechanics geometry optimization scheme of equilibrium structures and transition states. Journal of Computational Chemistry, 16, 1170-1179.
45. Matos, K.S., Mancini, D.T., da Cunha, E.F.F., Ku.a, K., Franca, T.C.C., & Ramalho, T.C. (2011). Molecular aspects of the reactivation process of acetylcholinesterase inhibited by cyclosarin. Journal of the Brazilian Chemical Society, 22, 1999-2004.
46. Mehrnejad, F., & Zarei, M. (2010). Molecular dynamics simulation study of the interaction of piscidin 1 with DPPC bilayers: Structure.activity relationship. Journal of Biomolecular Structure & Dynamics, 27, 551-559.
47. Meynier, C., Guerlesquin, F., & Roche, P. (2009). Computational studies of human galectin-1: Role of conserved tryptophan residue in stacking interaction with carbohydrate ligands. Journal of Biomolecular Structure & Dynamics, 27, 49-57.
48. Mohan, S., Perry, J.J.P., Poulose, N., Nair, B.G., & Anilkumar, G. (2009). Homology modeling of GLUT4, an insulin regulated facilitated glucose transporter and docking studies with ATP and its inhibitors. Journal of Biomolecular Structure & Dynamics, 26, 455-464.
49. Nemukhim, A.V., Lushchekina, S.V., Bochenkova, A.V., Golubeva, A.A., & Varfolomeev, S.D. (2008). Characterization of a complete cycle of acetylcholinesterase catalysis by ab initio QM/MM modelin. Journal of Molecular Modeling, 14, 409-416.
50. Ordentlich, A., Barak, D., Kronman, C., Ariel, N., Segall, Y., Velan, B., & Shafferman, A. (1996). The architecture of human acetylcholinesterase active center probed by interactions with selected organophosphate inhibitors. Journal of Biological Chemistry, 271(20), 11953-11962.
51. Quinn, D.M. (1987). Acetylcholinesterase: Enzyme structure, reaction dynamics, and virtual transition states. Chemical Reviews, 87, 955-975.
52. Ramalho, T.C., Caetano, M.S., Cunha, E.F.F., Souza, T.C.S., & Rocha, M.V.J. (2009). Construction and assessment of reaction models of class I EPSP synthase: Molecular docking and density functional theoretical calculations. Journal of Biomolecular Structure & Dynamics, 27, 195-207.
53. Ramalho, T.C., Franca, T.C.C., Renno, M.N., Guimaraes, A.P., Cunha, E.F.F., & Ku.a, K. (2010). Development of new acetylcholinesterase reactivators: Molecular modeling versus in vitro data. Chemico-Biological Interactions, 185, 73-77.
54. Ramalho, T.C., & Taft, C.A. (2005). Thermal and solvent effects on the NMR and UV parameters of some bioreductive drugs. Journal of Chemical Physics, 123(5), 054319.
55. Rieping, W., Habeck, M., Bardiaux, B., Bernard, A., Malliavin, T.E., & Nilges, M. (2007). ARIA2: Automated NOE assignment and data integration in NMR structure calculation. Bioinformatics, 23, 381-382.
56. Roy, S., & Thakur, A.R. (2010). 20ns Molecular dynamics simulation of the antennapedia homeodomain-DnaA complex: Water interaction and DnaA structure analysis. Journal of Biomolecular Structure & Dynamics, 27, 443-455.
57. Schwieters, C.D., Kuszewski, J.J., & Clore, G.M. (2006). Using Xplor-NIH for NMR molecular structure determination. Progress in Nuclear Magnetic Resonance Spectroscopy, 48, 47-62.
58. Sharadadevi, A., & Nagaraj, R. (2010). A molecular dynamics study of human defensins HBD-1 and HNP-3 in water. Journal of Biomolecular Structure & Dynamics, 27, 541-550.
59. Sidell, F.R., Takafuji, E.T., & Franz, D.R. (Eds.). (1997). Medical aspects of chemical and biological warfare-textbook of military medicine. Washington, DC: Office of the Surgeon General, US Army.
60. Sharma, S., Sonavane, U.B., & Joshi, R.R. (2010). Molecular dynamics simulations of cyclohexyl modified peptide nucleic acids (PNA). Journal of Biomolecular Structure & Dynamics, 27, 663-676.
61. Sille, J., & Remko, M. (2009). Computational study of the sulfonylated amino acid hydroxamates binding to the zinc ion within the active site of carbonic anhydrase. Journal of Biomolecular Structure & Dynamics, 26, 431-444.
62. Somani, S.M., Solana, R.P., & Dube, S.N. (1992). Toxicology of nerve agents. In S.M. Somani (Ed.), Chemical warfare agents (pp. 67-123). San Diego, CA: Academic Press.
63. Sousa da Silva, A.W., & Vranken, W.F. (BMC Research Notes, in press). ACPYPE - AnteChamber python parser interface. http://www.ccpn.ac.uk/software/ ACPYPE-folder.
64. Steven, S.Z., Peterson, M.W., Hamza, A., Zhan, C.G., Cerasoli, D.M., & Chang, W.E. (2011). Computational characterization of how the VX nerve agent binds human serum paraoxonase 1. Journal of Molecular Modeling, 17, 97-109.
65. Tao, Y., Rao, Z.H., & Liu, S.Q. (2010). Insight derived from molecular dynamics simulation into substrate-induced changes in protein motions of proteinase K. Journal of Biomolecular Structure & Dynamics, 28, 143-158.
66. Thomsen, R., & Christensen, M.H. (2006). MolDock: A new technique for high-accuracy molecular docking. Journal of Medicinal Chemistry, 49, 3315-3321.
67. Timofeyeva, N.A., Koval, V.V., Knorre, D.G., Zharkov, D.O., Saparbaev, M.K., Fedorova, O.S. (2009). Conformational dynamics of human AP endonuclease in base excision and nucleotide incision repair pathways. Journal of Biomolecular Structure & Dynamics, 26, 637-652.
68. Varughese, J.F., Chalovich, J.M., & Li, Y. (2010). Molecular dynamics studies on troponin (TnI-TnT-TnC) complexes: Insight into the regulation of muscle contraction. Journal of Biomolecular Structure & Dynamics, 28, 159-174.
69. Vranken, W.F., Boucher, W., Stevens, T.J., Fogh, R.H., Pajon, A., Llinas, M., Laue, E.D. (2005). The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins: Structure, Function, and Bioinformatics, 59, 687-696.
70. Walker, R.C., Crowley, M.F., & Case, D.A. (2008). The implementation of a fast and accurate QM/MM potential method in amber. Journal of Computational Physics, 29, 1019-1031.
71. Wang, J., Wang, W., Kollman, P.A., & Case, D.A. (2006). Automatic atom type and bond type perception in molecular mechanical calculations. Journal of Molecular Graphics and Modelling, 25, 247-260.
72. Warren, D. (2002). The PyMOL molecular graphics system. San Carlos, CA: DeLano Scientific.
73. Wong, L., Radic, Z., Brüggemann, R.J.M., Hosea, N., Berman, H.A., & Taylor, P. (2000). Mechanism of oxime reactivation of acetylcholinesterase analyzed by chirality and mutagenesis. Biochemistry, 39, 5750-5757.
74. Worek, F., Aurbek, N., Koller, M., Becker, C., Eyer, P., & Thiermann, H. (2007). Kinetic analysis of reactivation and aging of human acetylcholinesterase inhibited by different phosphoramidates. Biochemical Pharmacology, 73(11), 1807-1817.
75. Zhang, J.P. (2009). Studies on the structural stability of rabbit prion probed by molecular dynamics simulations. Journal of Biomolecular Structure & Dynamics, 27, 159-162.
76. Zhong, L.H., & Xie, J.M. (2009). Investigation of the effect of glycosylation on human prion protein by molecular dynamics. Journal of Biomolecular Structure & Dynamics, 26, 525-533.