Ligand-based 3D QSAR analysis of reactivation potency of mono- and bis-pyridinium aldoximes toward VX-inhibited rat acetylcholinesterase

Journal of Molecular Graphics and Modelling

Volumn 56, Issue , 2015, Pages 113-129

  Dolezal, Rafael ^a,c   Korabecny, Jan ^a,b,c   Malinak, David ^a,d   Honegr, Jan ^a,d   Musilek, Kamil ^c   Kuca, Kamil ^a,c  

^a UNIVERSITY HOSPITAL HRADEC KRALOVE   (Czech Republic)

^b UNIVERSITY OF DEFENCE   (Czech Republic)

^c UNIVERSITY OF HRADEC KRALOVE   (Czech Republic)

^d VSB TECHNICAL UNIVERSITY OF OSTRAVA   (Czech Republic)

Author keywords

3D QSAR; Acetylcholinesterase; Computational chemistry; Molecular docking; Reactivators; VX

Indexed keywords

CATALYST ACTIVITY; LIGANDS; MOLECULAR GRAPHICS; MOLECULAR MODELING; NOISE ABATEMENT; QUANTUM CHEMISTRY; RATS; THREE DIMENSIONAL COMPUTER GRAPHICS;

3D-QSAR; ACETYLCHOLINESTERASE; MOLECULAR DOCKING; REACTIVATORS; VX;

COMPUTATIONAL CHEMISTRY;

ACETYLCHOLINESTERASE; ALDOXIME; ACHE PROTEIN, RAT; CHEMICAL WARFARE AGENT; CHOLINESTERASE INHIBITOR; CHOLINESTERASE REACTIVATOR; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; LIGAND; METHYLPHOSPHONOTHIOIC ACID S (2 DIISOPROPYLAMINOETHYL) O ETHYL ESTER; OXIME; PHOSPHOROTHIOIC ACID DERIVATIVE; PYRIDINIUM DERIVATIVE;

ARTICLE; COMPARATIVE MOLECULAR FIELD ANALYSIS; DRUG POTENCY; MOLECULAR DOCKING; MOLECULAR INTERACTION; NOISE REDUCTION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE STRUCTURE ACTIVITY RELATION; RAT; THREE DIMENSIONAL IMAGING; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; ENZYME ACTIVATION; KINETICS; MOLECULAR DYNAMICS; QUANTUM THEORY; THERMODYNAMICS;

RATTUS;

ACETYLCHOLINESTERASE; ANIMALS; CHEMICAL WARFARE AGENTS; CHOLINESTERASE INHIBITORS; CHOLINESTERASE REACTIVATORS; ENZYME ACTIVATION; GPI-LINKED PROTEINS; KINETICS; LIGANDS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; ORGANOTHIOPHOSPHORUS COMPOUNDS; OXIMES; PYRIDINIUM COMPOUNDS; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; QUANTUM THEORY; RATS; THERMODYNAMICS;

EID: 84936992377     PISSN: 10933263     EISSN: 18734243     Source Type: Journal    
DOI: 10.1016/j.jmgm.2014.11.010     Document Type: Article

References (74)

1. K. Starke Presynaptic receptors Annu. Rev. Pharmacol. Toxicol. 21 1981 7 30 10.1146/annurev.pa.21.040181.000255
2. M. Moshiri, E. Darchini-Maragheh, and M. Balali-Mood Advances in toxicology and medical treatment of chemical warfare nerve agents DARU 20 81 2012 10.1186/2008-2231-20-81
3. A. Watson, D. Opresko, R. Young, V. Hauschild, J. King, and K. Bakshi Organophosphate nerve agents R.C. Gupta, Handbook of Toxicology of Chemical Warfare Agents 2009 Academic Press Inc. London (Chapter 6)
4. J. Bajgar, J. Fusek, K. Kuca, L. Bartosova, and D. Jun Treatment of organophosphate intoxication using cholinesterase reactivators: facts and fiction Mini Rev. Med. Chem. 7 2007 461 466 10.2174/138955707780619581
5. N. Munro Toxicity of the organophosphate chemical warfare agents GA, GB, and VX: implications for public protection Environ. Health Perspect. 102 1994 18 38
6. M. Nagao, T. Takatori, Y. Matsuda, M. Nakajima, H. Iwase, and K. Iwadate Definitive evidence for the acute sarin poisoning diagnosis in the Tokyo subway Toxicol. Appl. Pharmacol. 144 1997 198 203 10.1006/taap.1997.8110
7. G.A. Meneely, and C.R. Wyttenbach Effects of the organophosphate insecticides diazinon and parathion on bobwhite quail embryos: skeletal defects and acetylcholinesterase activity J. Exp. Zool. 252 1989 60 70 10.1002/jez.1402520109
8. A. Nordberg, and A.L. Svensson Cholinesterase inhibitors in the treatment of Alzheimer's disease Drug Saf. 19 1998 465 480 10.2165/00002018-199819060-00004
9. J. Korabecny, R. Dolezal, P. Cabelova, A. Horova, E. Hruba, J. Ricny, L. Sedlacek, E. Nepovimova, K. Spilovska, M. Andrs, K. Musilek, V. Opletalova, V. Sepsova, D. Ripova, and K. Kuca 7-MEOTA-donepezil like compounds as cholinesterase inhibitors: synthesis, pharmacological evaluation, molecular modeling and QSAR studies Eur. J. Med. Chem. 82 42 2014 6 438 10.1016/j.ejmech.2014.05.066
10. P. Ambure, and K. Roy Advances in quantitative structure-relationship models of anti-Alzheimer's agents Expert Opin. Drug. Discov. 9 2014 697 723 10.1517/17460441.2014.909404
11. I.G. McKeith, D.W. Dickson, J. Lowe, M. Emre, J.T. O'Brien, H. Feldman, J. Cummings, J.E. Duda, C. Lippa, E.K. Perry, D. Aarsland, H. Arai, C.G. Ballard, B. Boeve, D.J. Burn, D. Costa, T. Del Ser, B. Dubois, D. Galasko, S. Gauthier, C.G. Goetz, E. Gomez-Tortosa, G. Halliday, L.A. Hansen, J. Hardy, T. Iwatsubo, R.N. Kalaria, D. Kaufer, R.A. Kenny, A. Korczyn, K. Kosaka, V.M. Lee, A. Lees, I. Litvan, E. Londos, O.L. Lopez, S. Minoshima, Y. Mizuno, J.A. Molina, E.B. Mukaetova-Ladinska, F. Pasquier, R.H. Perry, J.B. Schulz, J.Q. Trojanowski, and M.D.L.B. Yamada Consortium on, diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium Neurology 65 2005 1863 1872 10.1212/01.wnl.0000187889.17253.b1
12. L. Maggi, and R. Mantegazza Treatment of myasthenia gravis: focus on pyridostigmine Clin. Drug Investig. 31 2011 691 701 10.2165/11593300-000000000-00000
13. M.C. de Koning, M. van Grol, and D. Noort Peripheral site ligand conjugation to a non-quaternary oxime enhances reactivation of nerve agent-inhibited human acetylcholinesterase Toxicol. Lett. 206 2011 54 59 10.1016/j.toxlet.2011.04.004
14. F. Worek, H. Thiermann, L. Szinicz, and P. Eyer Kinetic analysis of interactions between human acetylcholinesterase, structurally different organophosphorus compounds and oximes Biochem. Pharmacol. 68 2004 2237 2248 10.1016/j.bcp.2004.07.038
15. M. Jokanovic, and M. Prostran Pyridinium oximes as cholinesterase reactivators. Structure-activity relationship and efficacy in the treatment of poisoning with organophosphorus compounds Curr. Med. Chem. 16 2009 2177 2188 10.2174/092986709788612729
16. E. Carletti, H. Li, B. Li, F. Ekstrom, Y. Nicolet, M. Loiodice, E. Gillon, M.T. Froment, O. Lockridge, L.M. Schopfer, P. Masson, and F. Nachon Aging of cholinesterases phosphylated by tabun proceeds through O-dealkylation J. Am. Chem. Soc. 130 2008 16011 16020 10.1021/ja804941z
17. R.M. Dawson Review of oximes available for treatment of nerve agent poisoning J. Appl. Toxicol. 14 1994 317 331 10.1002/jat.2550140502
18. G. Mercey, T. Verdelet, J. Renou, M. Kliachyna, R. Baati, F. Nachon, L. Jean, and P.Y. Renard Reactivators of acetylcholinesterase inhibited by organophosphorus nerve agents Acc. Chem. Res. 45 2012 756 766 10.1021/ar2002864
19. J. Korabecny, O. Soukup, R. Dolezal, K. Spilovska, E. Nepovimova, M. Andrs, T. Duong Nguyen, D. Jun, K. Musilek, and M. Kucerova-Chlupacova From pyridinium-based to centrally active acetylcholinesterase reactivators Mini Rev. Med. Chem. 14 2014 215 221
20. D.E. Lorke, and G.A. Petroianu Minireview: does in-vitro testing of oximes help predict their in-vivo action after paraoxon exposure? J. Appl. Toxicol. 29 2009 459 469 10.1002/jat.1457
21. G.F. Makhaeva, E.V. Radchenko, I.I. Baskin, V.A. Palyulin, R.J. Richardsonc, and N.S. Zefirov Combined QSAR studies of inhibitor properties of O-phosphorylated oximes toward serine esterases involved in neurotoxicity, drug metabolism and Alzheimer's disease SAR QSAR Environ. Res. 23 62 2012 7 647 10.1080/1062936X.2012.679690
22. K. Musilek, M. Komloova, O. Holas, A. Horova, M. Pohanka, F. Gunn-Moore, V. Dohnal, M. Dolezal, and K. Kuca Mono-oxime bisquaternary acetylcholinesterase reactivators with prop-1,3-diyl linkage - preparation, in vitro screening and molecular docking Bioorg. Med. Chem. 19 75 2011 4 762 10.1016/j.bmc.2010.12.021
23. O. Holas, K. Musilek, A. Horova, V. Opletalova, and K. Kuca SAR study on reactivators of ethyl-paraoxon inhibited acetylcholinesterase Lett. Drug Des. Discov. 9 2012 587 594 10.2174/157018012800673083
24. F. Worek, T. Wille, M. Koller, and H. Thiermann Reactivation kinetics of a series of related bispyridinium oximes with organophosphate-inhibited human acetylcholinesterase - structure-activity relationships Biochem. Pharmacol. 83 2012 1700 1706 10.1016/j.bcp.2012.03.002
25. K. Musilek, M. Dolezal, F. Gunn-Moore, and K. Kuca Design, evaluation and structure-activity relationship studies of the AChE reactivators against organophosphorus pesticides Med. Res. Rev. 31 2011 548 575 10.1002/med.20192
26. N. Aurbek, N.M. Herkert, M. Koller, H. Thiermann, and F. Worek Kinetic analysis of interactions of different sarin and tabun analogues with human acetylcholinesterase and oximes: is there a structure-activity relationship? Chem. Biol. Interact. 187 2010 215 219 10.1016/j.cbi.2010.01.035
27. K. Kuca, V. Racakova, D. Jun, and J. Bajgar Structure-activity relationship of acetylcholinesterase reactivators - antidotes against nerve agents Lett. Org. Chem. 4 2007 212 217 10.2174/157017807780737282
28. A.P. Guimaraes, T.C.C. Franca, T.C. Ramalho, M.N. Renno, E.F.F. da Cunha, K.S. Matos, D.T. Mancini, and K. Kuca Docking studies and effects of syn-anti isometry of oximes derived from pyridine imidazol bicycled systems as potential human acetylcholinesterase reactivators J. Appl. Biomed. 9 2011 163 171 10.2478/v10136-009-0037-1
29. T.C. Ramalho, C.C. Tanos, M.N. Renno, A.P. Guimaraes, E.F. da Cunha, and K. Kuca Development of new acetylcholinesterase reactivators: molecular modeling versus in vitro data Chem. Biol. Interact. 187 2010 436 440 10.1016/j.cbi.2010.05.016
30. A.K. Bhattacharjee, K. Kuca, K. Musilek, and R.K. Gordon In silico pharmacophore model for tabun-inhibited acetylcholinesterase reactivators: a study of their stereoelectronic properties Chem. Res. Toxicol. 23 2010 26 36 10.1021/tx900192u
31. H.M. Greenblatt, H. Dvir, I. Silman, and J.L. Sussman Acetylcholinesterase: a multifaceted target for structure-based drug design of anticholinesterase agents for the treatment of Alzheimer's disease J. Mol. Neurosci. 20 2003 369 383 10.1385/JMN:20:3:369
32. Y.P. Pang, T.M. Kollmeyer, F. Hong, J.C. Lee, P.I. Hammond, S.P. Haugabouk, and S. Brimijoin Rational design of alkylene-linked bis-pyridiniumaldoximes as improved acetylcholinesterase reactivators Chem. Biol. 10 2003 491 502 10.1016/S1074-5521(03)00126-1
33. M.L. Connolly Computation of molecular volume J. Am. Chem. Soc. 107 1985 1118 1124 10.1021/ja00291a006
34. D.M. Maxwell, I. Koplovitz, F. Worek, and R.E. Sweeney A structure-activity analysis of the variation in oxime efficacy against nerve agents Toxicol. Appl. Pharmacol. 231 2008 157 164 10.1016/j.taap.2008.04.007
35. D.M. Maxwell, K.M. Brecht, and R.E. Sweeney A common mechanism for resistance to oxime reactivation of acetylcholinesterase inhibited by organophosphorus compounds Chem.-Biol. Interact. 203 2013 72 76 10.1016/j.cbi.2012.08.024
36. E.X. Esposito, T.R. Stouch, T.R. Stouch, T. Wymore, and J.D. Madura Exploring the physicochemical properties of oxime-reactivation therapeutics for cyclosarin, sarin, tabun, and VX inactivated acetylcholinesterase Chem. Res. Toxicol. 27 9 2014 9 110 10.1021/tx400350b
37. V. Dohnal, K. Kuca, and D. Jun Prediction of a new broad-spectrum reactivator capable of reactivating acetylcholinesterase inhibited by nerve agents J. Appl. Biomed. 3 2005 139 145
38. P. Tosco, and T. Balle Open3DQSAR: a new open-source software aimed at high-throughput chemometric analysis of molecular interaction fields J. Mol. Model. 17 2011 201 208 10.1007/s00894-010-0684-x
39. K. Kuca, K. Musilek, D. Jun, J. Karasova, O. Soukup, J. Pejchal, and M. Hrabinova Structure-activity relationship for the reactivators of acetylcholinesterase inhibited by nerve agent VX Med. Chem. 9 2013 689 693
40. J. Bajgar, J. Fusek, J. Kassa, D. Jun, K. Kuca, and P. Hajek An attempt to assess functionally minimal acetylcholinesterase activity necessary for survival of rats intoxicated with nerve agents Chem. Biol. Interact. 175 2008 281 285 10.1016/j.cbi.2008.05.015
41. HyperChem(TM) Professional 7.52, Hypercube, Inc., 1115 NW 4th Street, Gainesville, Florida 32601, USA.
42. R.G. Parr Density functional theory Annu. Rev. Phys. Chem. 34 1983 631 656 10.1146/annurev.pc.34.100183.003215
43. M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb, J.R. Cheeseman, G. Scalmani, V. Barone, B. Mennucci, G.A. Petersson, H. Nakatsuji, M. Caricato, X. Li, H.P. Hratchian, A.F. Izmaylov, J. Bloino, G. Zheng, J.L. Sonnenberg, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, T. Vreven, J.A. Montgomery Jr., J.E. Peralta, F. Ogliaro, M. Bearpark, J.J. Heyd, E. Brothers, K.N. Kudin, V.N. Staroverov, T. Keith, R. Kobayashi, J. Normand, K. Raghavachari, A. Rendell, J.C. Burant, S.S. Iyengar, J. Tomasi, M. Cossi, N. Rega, J.M. Millam, M. Klene, J.E. Knox, J.B. Cross, V. Bakken, C. Adamo, J. Jaramillo, R. Gomperts, R.E. Stratmann, O. Yazyev, A.J. Austin, R. Cammi, C. Pomelli, J.W. Ochterski, R.L. Martin, K. Morokuma, V.G. Zakrzewski, G.A. Voth, P. Salvador, J.J. Dannenberg, S. Dapprich, A.D. Daniels, O. Farkas, J.B. Foresman, J.V. Ortiz, J. Cioslowski, and D.J. Fox Gaussian 09, Revision C.01 2010 Gaussian, Inc. Wallingford, CT
44. The PyMOL Molecular Graphics System, Version 1.5.0.4 Schrödinger, LLC.
45. P. Tosco, T. Balle, and F. Shiri Open3DALIGN: an open-source software aimed at unsupervised ligand alignment J. Comput. Aided Mol. Des. 25 2011 777 783 10.1007/s10822-011-9462-9
46. TINKER -software tools for molecular design, version 5.1; http://dasher.wustl.edu/tinker/ (accessed 13.06.13).
47. A.R. Leach, V.J. Gillet, R.A. Lewis, and R. Taylor Three-dimensional pharmacophore methods in drug discovery J. Med. Chem. 53 2010 539 558 10.1021/jm900817u
48. J. Taminau, G. Thijs, and H. De Winter Pharao: pharmacophore alignment and optimization J. Mol. Graph. Model. 27 2008 161 169 10.1016/j.jmgm.2008.04.003
49. N.J. Richmond, P. Willett, and R.D. Clark Alignment of three-dimensional molecules using an image recognition algorithm J. Mol. Graph. Model. 23 2004 199 209 10.1016/j.jmgm.2004.04.004
50. http://sourceforge.net/projects/open3dalign/files/source/
51. R. Jonker, and A. Volgenant A shortest augmenting path algorithm for dense and sparse linear assignment problems Computing 38 1987 325 340 10.1007/BF02278710
52. T.A. Halgren Merck molecular force field. II. MMFF94 van der Waals and electrostatic parameters for intermolecular interactions J. Comput. Chem. 17 1996 520 552 10.1002/(SICI)1096-987X(199604)17:5/6<520::AID-JCC2>3.0.CO;2-W
53. M. Baroni, G. Costantino, G. Cruciani, D. Riganelli, R. Valigi, and S. Clementi Generating optimal linear PLS estimations (GOLPE): an advanced chemometric tool for handling 3D-QSAR problems Quant. Struct.-Act. Relat. 12 1993 9 20 10.1002/qsar.19930120103
54. M.A. Kastenholz, M. Pastor, G. Cruciani, E.E. Haaksma, and T. Fox GRID/CPCA: a new computational tool to design selective ligands J. Med. Chem. 43 2000 3033 3044 10.1021/jm000934y
55. S. Wold, M. Sjostrom, and L. Eriksson PLS-regression: a basic tool of chemometrics Chemometr. Intell. Lab. 58 2001 109 130 10.1016/S0169-7439(01)00155-1
56. J. Verma, V.M. Khedkar, and E.C. Coutinho 3D-QSAR in drug design - a review Curr. Top. Med. Chem. 10 2010 95 115 10.2174/156802610790232260
57. R.D. Cramer III Partial least squares (PLS): its strengths and limitations Perspect. Drug Discov. Des. 1 1993 269 278 10.1007/BF02174528
58. P. Tosco, and T. Balle A 3D-QSAR-driven approach to binding mode and affinity prediction J. Chem. Inf. Model. 52 2012 302 307 10.1021/ci200411s
59. M. Pastor, G. Cruciani, and S. Clementi Smart region definition: a new way to improve the predictive ability and interpretability of three-dimensional quantitative structure-activity relationships J. Med. Chem. 40 1997 1455 1464 10.1021/jm9608016
60. M. Baroni, S. Clementi, G. Cruciani, G. Costantino, D. Riganelli, and E. Oberrauch Predictive ability of regression models. Part II: Selection of the best predictive PLS model J. Chemometr. 6 1992 347 356 10.1002/cem.1180060605
61. G.E.P. Box, and J.S. Hunter The 2 k-p fractional factorial designs Technometrics 3 1961 311 351
62. V. Centner, D.L. Massart, O.E. de Noord, S. de Jong, B.M. Vandeginste, and C. Sterna Elimination of uninformative variables for multivariate calibration Anal. Chem. 68 1996 3851 3858 10.1021/ac960321m
63. R. Gieleciak, and J. Polanski Modeling robust QSAR. 2. Iterative variable elimination schemes for CoMSA: application for modeling benzoic acid pKa values J. Chem. Inf. Model. 47 2007 547 556 10.1021/ci600295z
64. R. Grohmann, and T. Schindler Toward robust QSPR models: synergistic utilization of robust regression and variable elimination J. Comput. Chem. 29 2008 847 860 10.1002/jcc.20831
65. V. Consonni, D. Ballabio, and R. Todeschini Evaluation of model predictive ability by external validation techniques J. Chemometr. 24 2010 194 201 10.1002/cem.1290
66. R.D. Clark, and P.C. Fox Statistical variation in progressive scrambling J. Comput. Aided Mol. Des. 18 2004 563 576 10.1007/s10822-004-4077-z
67. A.C. Cameron, and F.A.G. Windmeijer An R-squared measure of goodness of fit for some common nonlinear regression models J. Econom. 77 1997 329 342 10.1016/S0304-4076(96)01818-0
68. G. Tóth, Z. Bodai, and K. Héberger Estimation of influential points in any data set from coefficient of determination and its leave-one-out cross-validated counterpart J. Comput. Aided Mol. Des. 27 2013 837 844 10.1007/s10822-013-9680-4
69. A. Golbraikh, and A. Tropsha Beware of q2! J. Mol. Graph. Model. 20 2002 269 276 10.1016/S1093-3263(01)00123-1
70. A. Cherkasov, E.N. Muratov, D. Fourches, A. Varnek, I.I. Baskin, M. Cronin, J. Dearden, P. Gramatica, Y.C. Martin, R. Todeschini, V. Consonni, V.E. Kuz'min, R. Cramer, R. Benigni, C. Yang, J. Rathman, L. Terfloth, J. Gasteiger, A. Richard, and A. Tropsha QSAR modeling: where have you been? Where are you going to? J. Med. Chem. 57 2014 4977 5010 10.1021/jm4004285
71. O. Trott, and A.J. Olson AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31 2010 455 461 10.1002/jcc.21334
72. M. Kliachyna, G. Santoni, V. Nussbaum, J. Renou, B. Sanson, J.-P. Colletier, M. Arboléas, M. Loiodice, M. Weik, L. Jean, P.-Y. Renard, F. Nachon, and R. Baati Design, synthesis and biological evaluation of novel tetrahydroacridine pyridine-aldoxime and -amidoxime hybrids as efficient uncharged reactivators of nerve agent-inhibited human acetylcholinesterase Eur. J. Med. Chem. 78 2014 455 467 10.1016/j.ejmech.2014.03.044
73. P.I. Hammond, C. Kern, F. Hong, T.M. Kollmeyer, Y.P. Pang, and S. Brimijoin Cholinesterase reactivation in vivo with a novel bis-oxime optimized by computer-aided design J. Pharmacol. Exp. Ther. 307 2003 190 196 10.1124/jpet.103.053405
74. H. Zeng, and H. Zhang Combined 3D-QSAR modeling and molecular docking study on 1,4-dihydroindeno[1,2-c]pyrazoles as VEGFR-2 kinase inhibitors J. Mol. Graph. Model. 29 2010 54 71 10.1016/j.jmgm.2010.04.004