Modeling reactivation of the phosphorylated human butyrylcholinesterase by QM(DFTB)/MM calculations

Journal of Theoretical and Computational Chemistry

Volumn 14, Issue 7, 2015, Pages

  Kulakova, Anna ^a   Lushchekina, Sofya ^b   Grigorenko, Bella ^a,b   Nemukhin, Alexander ^a,b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b EMANUEL INSTITUTE OF BIOCHEMICAL PHYSICS   (Russian Federation)

Author keywords

Human butyrylcholinesterase; molecular modeling; mutants; QM MM

Indexed keywords

EID: 84949533946     PISSN: 02196336     EISSN: None     Source Type: Journal    
DOI: 10.1142/S0219633615500510     Document Type: Article

References (34)

1. Massoulie J, Sussman J, Bon S, Silman I, Structure and functions of acetylcholinesterase and butyrylcholinesterase, Prog Brain Res 98:139-146, 1993.
2. Masson P, Lockridge O, Butyrylcholinesterase for protection from organophosphorus poisons: Catalytic complexities and hysteretic behavior, Arch Biochem Biophys 494:107-120, 2010.
3. Nachon F, Brazzolotto X, Trovaslet M, Masson P, Progress in the development of enzyme-based nerve agent bioscavengers, Chem Biol Interact 206:536-544, 2013.
4. Field M, Wymore TW, Multiscale modeling of nerve agent hydrolysis mechanisms: A tale of two Nobel Prizes, Phys Scr 89:108004, 2014.
5. Amitay M, Shurki A, The structure of G117H mutant of butyrylcholinesterase: Nerve agents scavenger, Proteins 77:370-377, 2009.
6. Amitay M, Shurki A, Hydrolysis of organophosphate compounds by mutant butyrylcholinesterase: A story of two histidines, Proteins 79:352-364, 2011.
7. Yao Y, Liu J, Zhan CG, Why does the G117H mutation considerably improve the activity of human butyrylcholinesterase against sarin? Insights from quantum mechanical/molecular mechanical free energy calculations, Biochemistry 51:8980-8992, 2012.
8. Millard CB, Lockridge O, Broomfield CA, Design and expression of organophosphorus acid anhydride hydrolase activity in human butyrylcholinesterase, Biochemistry 34:15925-15933, 1995.
9. Lockridge O, Blong RM, Masson P, Froment MT, Millard CB, Broomfield CA, A single amino acid substitution, Gly117His, confers phosphotriesterase (organophosphorus acid anhydride hydrolase) activity on human butyrylcholinesterase, Biochemistry 36:786-795, 1997.
10. Kovach IM, Structure and dynamics of serine hydrolase-organophosphate adducts, J Enzyme Inhib 2:199-208, 1988.
11. Masson P, Cléry C, Guerra P, Redslob A, Albaret C, Fortier PL, Hydration change during the aging of phosphorylated human butyrylcholinesterase: Importance of residues aspartate-70 and glutamate-197 in the water network as probed by hydrostatic and osmotic pressures, Biochem J 343:361-369, 1999.
12. Nachon F, Asojo OA, Borgstahl GEO, Masson P, Lockridge O, Role of water in aging of human butyrylcholinesterase inhibited by ecothiophate: The crystal structure suggests two alternative mechanisms of aging, Biochemistry 44:1154-1162, 2005.
13. Nachon F, Carletti E, Wandhammer M, Nicolet Y, Schopfer LM, Masson P, Lockridge O, X-ray crystallographic snapshots of reaction intermediates in the G117H mutant of human butyrylcholinesterase, a nerve agent target engineered into a catalytic bioscavenger, Biochem J 434:73-82, 2011.
14. Aqvist J, Warshel A, Simulation of enzyme-reactions using valence bond force-fields and other hybrid quantum-classical approaches, Chem Rev 93:2523-2544, 1993.
15. Elstner M, Porezag D, Jungnickel G, Elsner J, Haugk M, Frauenheim T, Suhai S, Seifert G, Self-consistent-charge density-functional tight-binding method for simulations of complex materials properties, Phys Rev B 58:7260-7268, 1998.
16. Li GH, Cui Q, Mechanochemical coupling in myosin: A theoretical analysis with molecular dynamics and combined QM/MM reaction path calculations, J Phys Chem B 108:3342-3357, 2004.
17. Yu H, Ma L, Yang Y, Cui Q, Mechanochemical coupling in myosin motor domain: I. Equilibrium active site simulations. PLoS Comput Biol 3:0199-0213, 2007.
18. Yang Y, Yu HB, Cui Q, Extensive conformational transitions are required to turn on ATP hydrolysis in myosin, J Mol Biol 381:1407-1420, 2008.
19. Xia F, Rudack T, Cui Q, Kötting C, Gerwert K, Detailed structure of the H2PO + 4 guanosine diphosphate intermediate in Ras-GAP decoded from FTIR experiments by biomolecular simulations, J Am Chem Soc 134:20041-20044, 2012.
20. Liang R, Swanson JM, Voth GA, Benchmark study of the SCC-DFTB approach for a biomolecular proton channel, J Chem Theory Computat 10:451-462, 2014.
21. Case DA, Cheatham T, Darden T, Gohlike H, Luo R, Merz KM, Onufriev A, Simmerling C, Wang B, Woods R, The Amber biomolecular simulation programs, J Comput Chem 26:1668-1688, 2005.
22. Seabra GM, Walker RC, Elstner M, Case DA, Roitberg AE, Implementation of the SCCDFTB method for hybrid QM/MM simulations within the Amber molecular dynamics package, J Phys Chem A 111:5655-5664, 2007.
23. Qian N, Kovach IM, Key active site residues in the inhibition of acetylcholinesterases by soman, FEBS Lett 336:263-266, 1993.
24. Viragh C, Akhmetshin R, Kovach IM, Broomfield C, Unique pushpull mechanism of dealkylation in soman-inhibited cholinesterases, Biochemistry 36:8243-8252, 1997.
25. Nemukhin AV, Lushchekina SV, Bochenkova AV, Golubeva AA, Varfolomeev SD, Characterization of a complete cycle of acetylcholinesterase catalysis by ab initio QM/MM modeling, J Mol Model 14:409-416, 2008.
26. Nemukhin AV, Grigorenko BL, Morozov DI, Kochetov MS, Lushchekina SV, Varfolomeev SD, On quantum mechanical-molecular mechanical (QM/MM) approaches to model hydrolysis of acetylcholine by acetylcholinesterase, Chem Biol Interact 203:51-56, 2013.
27. Correa-Basurto J, Bello M, Rosales-Hernández MC, Hernández-Rodríguez M, Nicolás-Vázquez I, Rojo-Domínguez A, Trujillo-Ferrara JG, Miranda R, Flores-Sandoval CA, QSAR, docking, dynamic simulation and quantum mechanics studies to explore the recognition properties of cholinesterase binding sites, Chem Biol Interact 209:1-13, 2014.
28. Correa-Basurto J, Flores-Sandoval C, Marin-Cruz J, Rojo-Domínguez A, Espinoza-Fonseca LM, Trujillo-Ferrara JG, Docking and quantum mechanic studies on cholinesterases and their inhibitors, Eur J Med Chem 42:10-19, 2007.
29. Gonalves AS, Frana TCC, Caetano MS, Ramalho TC, Reactivation steps by 2-PAM of tabun-inhibited human acetylcholinesterase: Reducing the computational cost in hybrid QM/MM methods, J Biomol Struct Dyn 32:301-307, 2014.
30. Qiao Y, Han K, Zhan CG, Reaction pathways and free energy profiles for cholinesterasecatalyzed hydrolysis of 6-monoacetylmorphine, Org Biomol Chem 12:2214-2227, 2014.
31. Yang Y, Yu H, York D, Elstner M, Cui Q, Description of phosphate hydrolysis reactions with the self-consistent-charge density-functional-tight-binding (SCC-DFTB) theory. 1. Parameterization, J Chem Theory Computat 4:2067-2084, 2008.
32. Gaus M, Cui Q, Elstner M, DFTB3: Extension of the self-consistent-charge densityfunctional tight-binding method (SCC-DFTB), J Chem Theory Computat 7:931-948, 2011.
33. Gaus M, Lu X, Elstner M, Cui Q, Parameterization of DFTB3/3OB for sulphur and phosphorus for chemical and bilogical applications, J Chem Theory Computat 10:1518-1537, 2014.
34. Voevodin VV, Zhumatiy SA, Sobolev SI, Antonov AS, Bryzgalov PA, Nikitenko DA, Stefanov KS, Voevodin VV, Practice of \Lomonosov" supercomputer, Open Syst J, (Moscow) 7:36-39, 2012.