New insights on the molecular recognition of imidacloprid with aplysia californica AChBP: A computational study

Journal of Physical Chemistry B

Volumn 117, Issue 15, 2013, Pages 3944-3953

  Cerón Carrasco, José P ^a   Jacquemin, Denis ^a,b   Graton, Jéroîme ^a   Thany, Steeve ^c   Le Questel, Jean Yves ^a  

^a UNIVERSITÉ DE NANTES   (France)

^b INSTITUT UNIVERSITAIRE DE FRANCE   (France)

^c UNIVERSITÉ D'ANGERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; HYDROGEN BONDS; IONS; MOLECULAR RECOGNITION; VAN DER WAALS FORCES;

ACETYLCHOLINE-BINDING PROTEINS; COMPUTATIONAL STUDIES; EXTRACELLULAR DOMAINS; NEONICOTINOID INSECTICIDES; NICOTINIC ACETYLCHOLINE RECEPTORS; NON-COVALENT INTERACTION; PAIRWISE INTERACTION; VAN DER WAALS INTERACTIONS;

INSECTICIDES;

EID: 84876463514     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp310242n     Document Type: Article

References (63)

1. Corringer, P. J.; Le Novere, N.; Changeux, J. P. Nicotinic Receptors at the Amino Acid Level Annu. Rev. Pharmacol. Toxicol. 2000, 40, 431-458
2. Karlin, A. Emerging Structure of the Nicotinic Acetylcholine Receptors Nat. Rev. Neurosci. 2002, 3, 102-114
3. Grutter, T.; Changeux, J. P. Nicotinic Receptors in Wonderland Trends Biochem. Sci. 2001, 26, 459-463
4. Matsuda, K.; Buckingham, S. D.; Kleier, D.; Rauh, J. J.; Grauso, M.; Sattelle, D. B. Neonicotinoids: Insecticides Acting on Insect Nicotinic Acetylcholine Receptors Trends Pharmacol. Sci. 2001, 22, 573-580
5. Matsuda, K.; Shimomura, M.; Ihara, M.; Akamatsu, M.; Sattelle, D. B. Neonicotinoids Show Selective and Diverse Actions on Their Nicotinic Receptor Targets: Electrophysiology, Molecular Biology, and Receptor Modeling Studies Biosci. Biotechnol. Biochem. 2005, 69, 1442-1452
6. Tomizawa, M.; Casida, J. E. Selective Toxicity of Neonicotinoids Attributable to Specificity of Insect and Mammalian Nicotinic Receptors Annu. Rev. Entomol. 2003, 48, 339-364
7. Jeschke, P.; Nauen, R. Neonicotinoids: From Zero to Hero in Insecticide Chemistry Pest. Manag. Sci. 2008, 64, 1084-1098
8. Jeschke, P.; Nauen, R.; Schindler, M.; Elbert, A. Overview of the Status and Global Strategy for Neonicotinoids J. Agric. Food Chem. 2011, 59, 2897-2908
9. Kagabu, S. Discovery of Imidacloprid and Further Developments from Strategic Molecular Designs J. Agric. Food Chem. 2011, 59, 2887-2896
10. Wells, G. B. Structural Answers and Persistent Questions about How Nicotinic Receptors Work Front. Biosci. 2008, 13, 5479-5510
11. Liu, Z. W.; Williamson, M. S.; Lansdell, S. J.; Denholm, I.; Han, Z. J.; Millar, N. S. A Nicotinic Acetylcholine Receptor Mutation Conferring Target-Site Resistance to Imidacloprid in Nilaparvata Lugens (Brown Planthopper) Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 8420-8425
12. Liu, Z.; Han, Z.; Zhang, Y.; Song, F.; Yao, X.; Liu, S.; Gu, J.; Millar, N. S. Heteromeric Co-assembly of Two Insect Nicotinic Acetylcholine Receptor Alpha Subunits: Influence on Sensitivity to Neonicotinoid Insecticides J. Neurochem. 2009, 108, 498-506
13. Liu, Z.; Han, Z.; Liu, S.; Zhang, Y.; Song, F.; Yao, X.; Gu, J. Amino Acids Outside of the Loops that Define the Agonist Binding Site Are Important for Ligand Binding to Insect Nicotinic Acetylcholine Receptors J. Neurochem. 2008, 106, 224-230
14. Tomizawa, M.; Casida, J. E. Molecular Recognition of Neonicotinoid Insecticides: The Determinants of Life or Death Acc. Chem. Res. 2009, 42, 260-269
15. Talley, T. T.; Harel, M.; Hibbs, R. E.; Radic, Z.; Tomizawa, M.; Casida, J. E.; Taylor, P. Atomic Interactions of Neonicotinoid Agonists with AChBP: Molecular Recognition of the Distinctive Electronegative Pharmacophore Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 7606-7611
16. Ihara, M.; Okajima, T.; Yamashita, A.; Oda, T.; Hirata, K.; Nishiwaki, H.; Morimoto, T.; Akamatsu, M.; Ashikawa, Y.; Kuroda, S.; Mega, R.; Kuramitsu, S.; Sattelle, D. B.; Matsuda, K. Crystal Structures of Lymnaea Stagnalis AChBP in Complex with Neonicotinoid Insecticides Imidacloprid and Clothianidin Invertebr. Neurosci. 2008, 8, 71-81
17. Davis, A. M.; St-Gallay, S. A.; Kleywegt, G. J. Limitations and Lessons in the Use of X-ray Structural Information in Drug Design Drug Discovery Today 2008, 13, 831-841
18. Liebeschuetz, J.; Hennemann, J.; Olsson, T.; Groom, C. R. The Good, the Bad and the Twisted: A Survey of Ligand Geometry in Protein Crystal Structures J. Comput.-Aided Mol. Des. 2012, 26, 169-183
19. Taly, A.; Colas, C.; Malliavin, T.; Blondel, A.; Nilges, M.; Corringer, P.-J.; Joseph, D. Discrimination of Agonists versus Antagonists of Nicotinic Ligands Based on Docking onto AChBP Structures J. Mol. Graphics Modell. 2011, 30, 100-109
20. Liu, G.-Y.; Ju, X.-L.; Cheng, J. Selectivity of Imidacloprid for Fruit Fly versus Rat Nicotinic Acetylcholine Receptors by Molecular Modeling J. Mol. Model. 2010, 16, 993-1002
21. Amiri, S.; Shimomura, M.; Vijayan, R.; Nishiwaki, H.; Akamatsu, M.; Matsuda, K.; Jones, A. K.; Sansom, M. S. P.; Biggin, P. C.; Sattelle, D. B. A Role for Leu118 of Loop E in Agonist Binding to the α7 Nicotinic Acetylcholine Receptor Mol. Pharmacol. 2008, 73, 1659-1667
22. Rocher, A.; Marchand-Geneste, N. Homology Modelling of the Apis Mellifera Nicotinic Acetylcholine Receptor (nAChR) and Docking of Imidacloprid and Fipronil Insecticides and Their Metabolites SAR QSAR Environ. Res. 2008, 19, 245-261
23. Tomizawa, M.; Talley, T. T.; Maltby, D.; Durkins, K. A.; Medzihradszky, K. F.; Burlingame, A. L.; Taylor, P.; Casida, J. E. Mapping the Elusive Neonicotinoid Binding Site Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 9075-9080
24. Li, X.; Li, Y.; Cheng, T. J.; Liu, Z. H.; Wang, R. X. Evaluation of the Performance of Four Molecular Docking Programs on a Diverse Set of Protein-Ligand Complexes J. Comput. Chem. 2010, 31, 2109-2125
25. Cross, J. B.; Thompson, D. C.; Rai, B. K.; Baber, J. C.; Fan, K. Y.; Hu, Y. B.; Humblet, C. Comparison of Several Molecular Docking Programs: Pose Prediction and Virtual Screening Accuracy J. Chem. Inf. Model. 2009, 49, 1455-1474
26. Guallar, V.; Wallrapp, F. H. QM/MM Methods: Looking Inside Heme Proteins Biochemistry Biophys. Chem. 2010, 149, 1-11
27. De Vivo, M. Bridging Quantum Mechanics and Structure-Based Drug Design Front. Biosci. 2011, 16, 1619-1633
28. Menikarachchi, L. C.; Gascón, J. A. QM/MM Approaches in Medicinal Chemistry Research Curr. Top. Med. Chem. 2010, 10, 46-54
29. Senn, H. M.; Thiel, W. QM/MM Methods for Biomolecular Systems Angew. Chem., Int. Ed. Engl. 2009, 48, 1198-1229
30. Wang, Y.; Cheng, J.; Qian, X.; Li, Z. Actions between Neonicotinoids and Key Residues of Insect nAChR Based on an Ab Initio Quantum Chemistry Study: Hydrogen Bonding and Cooperative π-π Interaction Bioorg. Med. Chem. 2007, 15, 2624-2630
31. Vreven, T.; Byun, K. S.; Komaromi, I.; Dapprich, S.; Montgomery, J. A., Jr.; Morokuma, K.; Frisch, M. J. Combining Quantum Mechanics Methods with Molecular Mechanics Methods in ONIOM J. Chem. Theory Comput. 2006, 2, 815-826
32. Kagabu, S.; Matsuno, H. Chloronicotinyl Insecticides. 8. Crystal and Molecular Structures of Imidacloprid and Analogous Compounds J. Agric. Food Chem. 1997, 45, 276-281
33. Chopra, D.; Mohan, T. P.; Rao, K. S.; Row, T. N. G. (2 E)-1-[(6-Chloropyridin-3-yl)methyl]- N -nitroimidazolidin-2-imine (Imidachloprid) Acta Crystallogr. 2004, E60, O2415-O2417
34. Le Questel, J.-Y.; Graton, J.; Cerón-Carrasco, J. P.; Jacquemin, D.; Planchat, A.; Thany, S. H. New Insights on the Molecular Features and Electrophysiological Properties of Dinotefuran, Imidacloprid and Acetamiprid Neonicotinoid Insecticides Bioorg. Med. Chem. 2011, 19, 7623-7634
35. Delano, W. L. The Pymol Molecular Graphics System; Delano Scientific: San Carlos, CA, 2004, (http://www.pymol.org).
36. Saen-oon, S.; Kuno, M.; Hannongbua, S. Binding Energy Analysis for Wild-Type and Y181C Mutant HIV-1 RT/8-Cl TIBO Complex Structures: Quantum Chemical Calculations Based on the ONIOM Method Proteins: Struct., Funct., Bioinf. 2005, 61, 859-869
37. Kitisripanya, N.; Saparpakorn, P.; Wolschann, P.; Hannongbua, S. Binding of Huperzine A and Galanthamine to Acetylcholinesterase, Based on ONIOM Method Nanomed-Nanotechnol. Biol. Med. 2011, 7, 60-68
38. Sponer, J.; Riley, K. E.; Hobza, P. Nature and Magnitude of Aromatic Stacking of Nucleic Acid Bases Phys. Chem. Chem. Phys. 2008, 10, 2595-2610
39. Hobza, P.; Sponer, J. Toward True DNA Base-Stacking Energies: MP2, CCSD(T), and Complete Basis Set Calculations J. Am. Chem. Soc. 2002, 124, 11802-11808
40. Zhao, Y.; Truhlar, D. G. Hybrid Meta Density Functional Theory Methods for Thermochemistry, Thermochemical Kinetics, and Noncovalent Interactions: The MPW1B95 and MPWB1K Models and Comparative Assessments for Hydrogen Bonding and van der Waals Interactions J. Phys. Chem. A 2004, 108, 6908-6918
41. Zhao, Y.; Truhlar, D. G. How Well Can New-Generation Density Functional Methods Describe Stacking Interactions in Biological Systems? Phys. Chem. Chem. Phys. 2005, 7, 2701-2705
42. Zhao, Y.; Schultz, N. E.; Truhlar, D. G. Density Functionals with Broad Applicability in Chemistry Acc. Chem. Res. 2008, 41, 157-167
43. Zhao, Y.; Truhlar, D. G. The M06 Suite of Density Functionals for Main Group Thermochemistry, Thermochemical Kinetics, Noncovalent Interactions, Excited States, and Transition Elements: Two New Functionals and Systematic Testing of Four M06-Class Functionals and 12 Other Functionals Theor. Chem. Acc. 2008, 120, 215-241
44. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Gaussian 09, revision A.02; Gaussian, Inc.: Wallingford, CT, 2009.
45. Stewart, J. J. P. Optimization of Parameters for Semiempirical Methods V: Modification of NDDO Approximations and Application to 70 Elements J. Mol. Model. 2007, 13, 1173-1213
46. Rutledge, L. R.; Wetmore, S. D. Modeling the Chemical Step Utilized by Human Alkyladenine DNA Glycosylase: A Concerted Mechanism Aids in Selectively Excising Damaged Purines J. Am. Chem. Soc. 2011, 133, 16258-16269
47. Stewart, J. J. P. Application of the PM6 Method to Modeling Proteins J. Mol. Model. 2009, 15, 765-805
48. Boonsri, P.; Kuno, M.; Hannongbua, S. Key Interactions of the Mutant HIV-1 Reverse Transcriptase/efavirenz: An Evidence Obtained from ONIOM Method Med. Chem. Commun. 2011, 2, 1181-1187
49. Boys, S.; Bernardi, F. The Calculations of Small Molecular Interaction by the Difference of Separate Total Energies. Some Procedures with Reduced Error Mol. Phys. 1970, 19, 553-566
50. Hankins, D.; Moskowitz, J. W. Water Molecule Interactions J. Chem. Phys. 1970, 53, 4544-4554
51. Dziekonski, P.; Sokalski, W. A.; Leszczynski, J. Physical Nature of Environmental Effects on Intermolecular Proton Transfer in (O2NOH· ··NH3)(H2O)n and (ClH···NH3)(H2O)n (n=1-3) Complexes Chem. Phys. 2001, 272, 37-45
52. Johnson, E. R.; Keinan, S.; Mori-Sánchez, P.; Contreras- García, J.; Cohen, A. J.; Yang, W. Revealing Noncovalent Interactions J. Am. Chem. Soc. 2010, 132, 6498-6506
53. Contreras-García, J.; Yang, W.; Johnson, E. R. Analysis of Hydrogen-Bond Interaction Potentials from the Electron Density: Integration of Noncovalent Interaction Regions J. Phys. Chem. A 2011, 115, 12983-12990
54. Contreras-García, J.; Johnson, E. R.; Keinan, S.; Chaudret, R.; Piquemal, J.-P.; Beratan, D. N.; Yang, W. NCIPLOT: A Program for Plotting Noncovalent Interaction Regions J. Chem. Theory Comput. 2001, 7, 625-632
55. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38
56. Sousa, S. F.; Fernandes, P. A.; Ramos, M. J. General Performance of Density Functionals J. Phys. Chem. A 2007, 111, 10439-10452
57. van der Wijst, T.; Fonseca-Guerra, C.; Swart, M.; Bickelhaupt, F. Performance of Various Density Functionals for the Hydrogen Bonds in DNA Base Pairs Chem. Phys. Lett. 2006, 426, 415-421
58. Matsuda, K.; Kanaoka, S.; Akamatsu, M.; Sattelle, D. B. Diverse Actions and Target-Site Selectivity of Neonicotinoids: Structural Insights Mol. Pharmacol. 2009, 76, 1-10
59. Perrin, C. L.; Nielson, J. B. "Strong" Hydrogen Bonds in Chemistry and Biology Annu. Rev. Phys. Chem. 1997, 48, 511-544
60. Zhang, W.; Yang, X.; Chen, W.; Xu, X.; Li, L.; Zhai, H.; Zhong, L. Design, Multicomponent Synthesis, and Bioactivities of Novel Neonicotinoid Analogues with 1,4-Dihydropyridine Scaffold J. Agric. Food Chem. 2010, 58, 2741-2745
61. Duan, H.; Zhang, W.; Zhao, J.; Liang, D.; Yang, X.; Jin, S. A Novel Halogen Bond and a Better-known Hydrogen Bond Cooperation of Neonicotinoid and Insect Nicotinic Acetylcholine Receptor Recognition J. Mol. Model. 2012, 18, 3867-3875
62. Metrangolo, P.; Resnati, G. Halogen Bonding: A Paradigm in Supramolecular Chemistry Chem.-Eur. J. 2001, 7, 2511-2519
63. Parisini, E.; Metrangolo, P.; Pilati, T.; Resnati, G.; Terraneo, G. Halogen Bonding in Halocarbon-Protein Complexes: A Structural Survey Chem. Soc. Rev. 2011, 40, 2267-2278