A comparative study of trypsin specificity based on QM/MM molecular dynamics simulation and QM/MM GBSA calculation

Journal of Biomolecular Structure and Dynamics

Volumn 33, Issue 12, 2015, Pages 2606-2618

  Chen, Jianzhong ^a   Wang, Jinan ^b   Zhang, Qinggang ^c   Chen, Kaixian ^b   Zhu, Weiliang ^b  

^a SHANDONG JIAOTONG UNIVERSITY   (China)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^c SHANDONG NORMAL UNIVERSITY   (China)

Author keywords

binding free energies; MM GBSA method, trypsin specificity; QM MM molecular dynamics simulations; semi empirical Hamiltonian

Indexed keywords

AMIDINE; ASPARTIC ACID; BENZAMIDINE; CYSTEINE; GLUTAMINE; GLYCINE; HISTIDINE; SERINE; SODIUM CHLORIDE; TRYPSIN; TRYPTOPHAN; ENZYME INHIBITOR; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; ENZYME INHIBITION; ENZYME SPECIFICITY; FOURIER TRANSFORMATION; GENERALIZED BORN SURFACE AREA; HYDROGEN BOND; INTERMETHOD COMPARISON; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; PREDICTION; PRIORITY JOURNAL; QUANTUM MECHANICS; ALGORITHM; BINDING COMPETITION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; METABOLISM; PROTEIN TERTIARY STRUCTURE; QUANTUM THEORY; THERMODYNAMICS;

ALGORITHMS; BINDING SITES; BINDING, COMPETITIVE; ENZYME INHIBITORS; HYDROGEN BONDING; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; QUANTUM THEORY; THERMODYNAMICS; TRYPSIN;

EID: 84954025760     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2014.1003146     Document Type: Article

References (69)

1. Abdel-Azeim, S., Li, X., Chung, L. W., & Morokuma, K. (2011). Zinc-Homocysteine binding in cobalamin-dependent methionine synthase and its role in the substrate activation: DFT, ONIOM, and QM/MM molecular dynamics studies. Journal of Computational Chemistry, 32, 3154-3167.
2. Bas, D. C., Rogers, D. M., & Jensen, J. H. (2008). Very fast prediction and rationalization of pKa values for protein-ligand complexes. Proteins: Structure, Function, and Bioinformatics, 73, 765-783.
3. Beeman, D. (1976). Some multistep methods for use in molecular dynamics calculations. Journal of Computational Physics, 20, 130-139.
4. Bode, W., Greyling, H. J., Huber, R., Otlewski, J., & Wilusz, T. (1989). The refined 2.0 Å X-ray crystal structure of the complex formed between bovine β-trypsin and CMTI-I, a trypsin inhibitor from squash seeds (Cucurbita maxima) topological similarity of the squash seed inhibitors with the carboxypeptidase A inhibitor from potatoes. FEBS Letters, 242, 285-292.
5. Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., ... Kollman, P. A. (2012). AMBER 12. San Francisco: University of California.
6. Chen, J., Liang Z., Wang W., Yi C., Zhang S., & Zhang Q. (2014) Revealing origin of decrease in potency of darunavir and amprenavir against HIV-2 relative to HIV-1 protease by molecular dynamics simulations. Scientific Reports 4, 6872; doi:6810.1038/srep06872
7. Chen, J., Wang, J., Zhu, W., & Li, G. (2013). A computational analysis of binding modes and conformation changes of MDM2 induced by p53 and inhibitor bindings. Journal of Computer-Aided Molecular Design, 27, 965-974.
8. Coleman, T. G., Mesick, H. C., & Darby, R. L. (1977). Numerical integration. Annals of Biomedical Engineering, 5, 322-328.
9. 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. Dewar, M. J., Zoebisch, E. G., Healy, E. F., & Stewart, J. J. (1985). Development and use of quantum mechanical molecular models. 76. AM1: A new general purpose quantum mechanical molecular model. Journal of the American Chemical Society, 107, 3902-3909.
11. Ding, L., Chung, L. W., & Morokuma, K. (2013). Reaction mechanism of photoinduced decarboxylation of the photoactivatable green fluorescent protein: An ONIOM(QM: MM) STUDY. The Journal of Physical Chemistry B, 117, 1075-1084.
12. Ding, Y., Mei, Y., & Zhang, J. Z. H. (2008). Quantum mechanical studies of residue-specific hydrophobic interactions in p53-MDM2 binding. The Journal of Physical Chemistry B, 112, 11396-11401.
13. Duan, L. L., Mei, Y., Zhang, Q. G., & Zhang, J. Z. (2009). Intra-protein hydrogen bonding is dynamically stabilized by electronic polarization. The Journal of Chemical Physics, 130, 115102.
14. Duan, L. L., Mei, Y., Zhang, D., Zhang, Q. G., & Zhang, J. Z. (2010). Folding of a Helix at room temperature is critically aided by electrostatic polarization of intraprotein hydrogen bonds. Journal of the American Chemical Society, 132, 11159-11164.
15. Egelrud, T., Brattsand, M., Kreutzmann, P., Walden, M., Vitzithum, K., Marx U., & Mägert, H. (2005). hK5 and hK7, two serine proteinases abundant in human skin, are inhibited by LEKTI domain 6. British Journal of Dermatology, 153, 1200-1203.
16. 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.
17. Fan, Y., Cembran, A., Ma, S., & Gao, J. (2013). Connecting protein conformational dynamics with catalytic function as illustrated in dihydrofolate reductase. Biochemistry, 52, 2036-2049.
18. Field, M. J., Bash, P. A., & Karplus, M. (1990). A combined quantum mechanical and molecular mechanical potential for molecular dynamics simulations. Journal of Computational Chemistry, 11, 700-733.
19. Frisch, M. J., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., ... Fox, D. J. (2009). Gaussian, Inc, Wallingford CT Gaussian 09 Revision C01. Wallingford, CT: Gaussian.
20. Gao, Y., Lu, X., Duan, L. L., Zhang, J. Z., & Mei, Y. (2011). Polarization of intraprotein hydrogen bond is critical to thermal stability of short helix. The Journal of Physical Chemistry B, 116, 549-554.
21. 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.
22. Golubkov, P. A., & Ren, P. (2006). Generalized coarse-grained model based on point multipole and Gay-Berne potentials. The Journal of Chemical Physics, 125, 064103.
23. Gräter, F., Schwarzl, S. M., Dejaegere, A., Fischer, S., & Smith, J. C. (2005). Protein/ligand binding free energies calculated with quantum mechanics/molecular mechanics. The Journal of Physical Chemistry B, 109, 10474-10483.
24. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., & Simmerling, C. (2006). Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins: Structure, Function, and Bioinformatics, 65, 712-725.
25. Hou, G., & Cui, Q. (2013). Stabilization of different types of transition states in a single enzyme active site: QM/MM analysis of enzymes in the alkaline phosphatase superfamily. Journal of the American Chemical Society, 135, 10457-10469.
26. Hou, T., McLaughlin, W. A., & Wang, W. (2007). Evaluating the potency of HIV-1 protease drugs to combat resistance. Proteins: Structure, Function, and Bioinformatics, 71, 1163-1174.
27. Hu, G., & Wang, J. (2014). Ligand selectivity of estrogen receptors by a molecular dynamics study. European Journal of Medicinal Chemistry, 74, 726-735.
28. Hu, G.-D., Zhu, T., Zhang, S.-L., Wang, D., & Zhang, Q.-G. (2010). Some insights into mechanism for binding and drug resistance of wild type and I50V V82A and I84V mutations in HIV-1 protease with GRL-98065 inhibitor from molecular dynamic simulations. European Journal of Medicinal Chemistry, 45, 227-235.
29. Ibrahim, M. A. A. (2011). Performance assessment of semiempirical molecular orbital methods in describing halogen bonding: quantum mechanical and quantum mechanical/molecular mechanical-molecular dynamics study. Journal of Chemical Information and Modeling, 51, 2549-2559.
30. Imhof, P., Noé, F., Fischer, S., & Smith, J. C. (2006). AM1/d Parameters for magnesium in metalloenzymes. Journal of Chemical Theory and Computation, 2, 1050-1056.
31. Jiao, D., Zhang, J., Duke, R. E., Li, G., Schnieders, M. J., & Ren, P. (2009). Trypsin-ligand binding free energies from explicit and implicit solvent simulations with polarizable potential. Journal of Computational Chemistry, 30, 1701-1711.
32. 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, 926-930.
33. Ke, Z., Wang, S., Xie, D., & Zhang, Y. (2009). Born-Oppenheimer ab Initio QM/MM molecular dynamics simulations of the hydrolysis reaction catalyzed by protein arginine deiminase 4. The Journal of Physical Chemistry B, 113, 16705-16710.
34. Keerthana, S., & Kolandaivel, P. (2014). Study of mutation and misfolding of Cu-Zn SOD1 protein. Journal of Biomolecular Structure & Dynamics, 33, 1-17. doi:10.1080/07391102.07392013.07865104
35. Leiros, H. K. S., Brandsdal, B. O., Andersen, O. A., Os, V., Leiros, I., Helland R., ... Smalås, A. O. (2004). Trypsin specificity as elucidated by LIE calculations, X-ray structures, and association constant measurements. Protein Science, 13, 1056-1070.
36. Li, H., Robertson, A. D., & Jensen, J. H. (2005). Very fast empirical prediction and rationalization of protein pKa values. Proteins: Structure, Function, and Bioinformatics, 61, 704-721.
37. Liebschner, D., Dauter, M., Brzuszkiewicz, A., & Dauter, Z. (2013). On the reproducibility of protein crystal structures: five atomic resolution structures of trypsin. Acta Crystallographica Section D Biological Crystallography, 69, 1447-1462.
38. Mares-Guia, M., & Shaw, E. (1965). Studies on the active center of trypsin the binding of amidines and guanidines as model of the substrate side chain. The Journal of Biological Chemistry, 240, 1579-1585.
39. Meher, B. R., Kumar, M. V. S., & Bandyopadhyay, P. (2014). Interchain hydrophobic clustering promotes rigidity in HIV-1 protease flap dynamics: New insights from molecular dynamics. Journal of Biomolecular Structure & Dynamics, 32, 899-915.
40. Miller, B. R., III, McGee, T. D., Swails, J. M., Homeyer, N., Gohlke, H., & Roitberg, A. E. (2012). MMPBSA. py: An efficient program for end-state free energy calculations. Journal of Chemical Theory and Computation, 8, 3314-3321.
41. Mitsudo, K., Jayakumar, A., Henderson, Y., Frederick, M. J., Kang, Y. A., Wang M., ... Clayman, G. L. (2003). Inhibition of serine proteinases plasmin, trypsin, subtilisin A, cathepsin G, and elastase by LEKTI: A kinetic analysis. Biochemistry, 42, 3874-3881.
42. Naray-Szabo, G. (1984). Quantum chemical calculation of the enzyme-ligand interaction energy for trypsin inhibition by benzamidines. Journal of the American Chemical Society, 106, 4584-4589.
43. Nishio, M., Umezawa, Y., Fantini, J., Weiss, M. S., & Chakrabarti, P. (2014). CH-π hydrogen bonds in biological macromolecules. Physical Chemistry Chemical Physics, 16, 12648-12683.
44. 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.
45. Ota, N., Stroupe, C., Ferreira-da-Silva, J., Shah, S. A., Mares-Guia, M., & Brunger, A. T. (1999). Non-Boltzmann thermodynamic integration (NBTI) for macromolecular systems: Relative free energy of binding of trypsin to benzamidine and benzylamine. Proteins: Structure, Function, and Genetics, 37, 641-653.
46. Patil, D. N., Chaudhary, A., Sharma, A. K., Tomar, S., & Kumar, P. (2012). Structural basis for dual inhibitory role of tamarind Kunitz inhibitor (TKI) against factor Xa and trypsin. FEBS Journal, 279, 4547-4564.
47. Rocha, G. B., Freire, R. O., Simas, A. M., & Stewart, J. J. (2006). RM1: A reparameterization of AM1 for H, C, N, O, P, S, F, Cl, Br, and I. Journal of Computational Chemistry, 27, 1101-1111.
48. Roe, D. R., & Cheatham, T. E., III (2013). PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9, 3084-3095.
49. Sitkoff, D., Sharp, K. A., & Honig, B. (1994). Accurate calculation of hydration free energies using macroscopic solvent models. The Journal of Physical Chemistry, 98, 1978-1988.
50. Smith, G. K., Ke, Z., Guo, H., & Hengge, A. C. (2011). Insights into the phosphoryl transfer mechanism of cyclin-dependent protein kinases from ab Initio QM/MM free-energy studies. The Journal of Physical Chemistry B, 115, 13713-13722.
51. Söderhjelm, P. R., Aquilante, F., & Ryde, U. (2009). Calculation of Protein-ligand interaction energies by a fragmentation approach combining high-level quantum chemistry with classical many-body effects. The Journal of Physical Chemistry B, 113, 11085-11094.
52. Stewart, J. J. (1989). Optimization of parameters for semiempirical methods I. Method. Journal of Computational Chemistry, 10, 209-220.
53. Stewart, J. J. (2007). Optimization of parameters for semiempirical methods V: Modification of NDDO approximations and application to 70 elements. Journal of Molecular Modeling, 13, 1173-1213.
54. Talhout, R., & Engberts, J. B. (2001). Thermodynamic analysis of binding of p-substituted benzamidines to trypsin. European Journal of Biochemistry, 268, 1554-1560.
55. 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.
56. Wang, J., Shao, Q., Xu, Z., Liu, Y., Yang, Z., Cossins, B. P., ... Zhu, W. (2013). Exploring transition pathway and free-energy profile of large-scale protein conformational change by combining normal mode analysis and umbrella sampling molecular dynamics. The Journal of Physical Chemistry B, 118, 134-143.
57. 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.
58. Wang, X., Wu, S., Xu, D., Xie, D., & Guo, H. (2011). Inhibitor and substrate binding by angiotensin-converting enzyme: quantum mechanical/molecular mechanical molecular dynamics studies. Journal of Chemical Information and Modeling, 51, 1074-1082.
59. Wang, J., Yang, H., Zuo, Z., Yan, X., Wang, Y., Luo X., ... Zhu, W. (2010). Molecular dynamics simulations on the mechanism of transporting methylamine and ammonia by ammonium transporter AmtB. The Journal of Physical Chemistry B, 114, 15172-15179.
60. Wong, K.-Y., Richard, J. P., & Gao, J. (2009). Theoretical analysis of kinetic isotope effects on proton transfer reactions between substituted α-methoxystyrenes and substituted acetic acids. Journal of the American Chemical Society, 131, 13963-13971.
61. Word, J. M., Lovell, S. C., Richardson, J. S., & Richardson, D. C. (1999). Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation. Journal of Molecular Biology, 285, 1735-1747.
62. 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 and Computation, 6, 337-343.
63. 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.
64. Xu, B., Shen, H., Zhu, X., & Li, G. (2011). Fast and accurate computation schemes for evaluating vibrational entropy of proteins. Journal of Computational Chemistry, 32, 3188-3193.
65. Yamane, J., Yao, M., Zhou, Y., Hiramatsu, Y., Fujiwara, K., Yamaguchi T., ... Takemoto, H. (2011). In-crystal affinity ranking of fragment hit compounds reveals a relationship with their inhibitory activities. Journal of Applied Crystallography, 44, 798-804.
66. Zhang, H. M., Wang, Y. Q., & Zhou, Q. H. (2009). Investigation of the interactions of quercetin and morin with trypsin. Luminescence, 24, 355-362.
67. Zhu, T., He, X., & Zhang, J. Z. (2012). Fragment density functional theory calculation of NMR chemical shifts for proteins with implicit solvation. Physical Chemistry Chemical Physics, 14, 7837-7845.
68. Zhu, T., Xiao, X., Ji, C., & Zhang, J. Z. (2013). A new quantum calibrated force field for zinc-protein complex. Journal of Chemical Theory and Computation, 9, 1788-1798.
69. Zhu, T., Zhang, J. Z., & He, X. (2013). Automated fragmentation QM/MM calculation of amide proton chemical shifts in proteins with explicit solvent model. Journal of Chemical Theory and Computation, 9, 2104-2114.