Steered molecular dynamics simulations reveal important mechanisms in reversible monoamine oxidase B inhibition

Biochemistry

Volumn 50, Issue 29, 2011, Pages 6441-6454

  Allen, William J ^a   Bevan, David R ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

, INHIBITOR; ACTIVE SITE; ATOMISTIC MOLECULAR DYNAMICS SIMULATIONS; AVERAGE ENERGY; BI-LAYER; BINDING POCKETS; BINDING PROCESS; DRUG TARGETS; ENZYME-INHIBITOR COMPLEX; MD SIMULATION; MEMBRANE PROTEINS; MONOAMINE OXIDASE B; NON EQUILIBRIUM; PARKINSONS DISEASE; STEERED MOLECULAR DYNAMICS SIMULATIONS;

BINDING ENERGY; COMPLEXATION; ENZYMES; LIPID BILAYERS;

MOLECULAR DYNAMICS;

1,4 DIPHENYL 2 BUTENE; 1H INDOLE 2,3 DIONE; 2 [4 (FLUOROBENZYLOXYBENZYLAMINO) PROPIONAMIDE]; 7 [(3 CHLOROBENZYL)OXY] 2 OXO 2H CHROMENE4 CARBALDEHYDE; 7 [(3 CHLOROBENZYL)OXY] 4 [(METHYLAMINO)METHYL] 2H CHROMEN 2 ONE; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; FARNESOL; MONOAMINE OXIDASE B INHIBITOR; N METHYL 1 AMINOINDAN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME BINDING; ENZYME INHIBITION; EQUILIBRIUM CONSTANT; LIPID BILAYER; MOLECULAR DYNAMICS; PARKINSON DISEASE; PRIORITY JOURNAL; SIMULATION;

CATALYTIC DOMAIN; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; MONOAMINE OXIDASE; MONOAMINE OXIDASE INHIBITORS; PROTEIN MULTIMERIZATION; THERMODYNAMICS;

EID: 79960522891     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200446w     Document Type: Article

References (52)

1. Shih, J. C., Chen, K., and Ridd, M. J. (1999) Monoamine oxidase: From genes to behavior Annu. Rev. Neurosci. 22, 197-217 (Pubitemid 29144886)
2. Fowler, J. S., Volkow, N. D., Wang, G.-J., Logan, J., Pappas, N., Shea, C., and Macgregor, R. (1997) Age-related increases in brain monoamine oxidase B in living healthy human subjects Neurobiol. Aging 18, 431-435 (Pubitemid 27435085)
3. Tabakman, R., Lecht, S., and Lazarovici, P. (2004) Neuroprotection by monoamine oxidase B inhibitors: a therapeutic strategy for Parkinsons disease? BioEssays 26, 80-90 (Pubitemid 38095352)
4. Birkmayer, W., Knoll, J., Riederer, P., Youdim, M. B., Hars, V., and Marton, J. (1985) Increased life expectancy resulting from addition of L-deprenyl to Madopar treatment in Parkinsons disease: a longterm study J. Neural Transm. 64, 113-127 (Pubitemid 16191073)
5. Finberg, J. P. M., Lamensdorf, I., Commissiong, J. W., and Youdim, M. B. H. (1996) Pharmacology and neuroprotective properties of rasagiline J. Neural Transm. 48, 95-101 (Pubitemid 26423350)
6. Naoi, M. and Maruyama, W. Functional mechanism of neuroprotection by inhibitors of type B monoamine oxidase in Parkinsons disease. Expert Rev. Neurother. 2009, not supplied.
7. Binda, C., Wang, J., Pisani, L., Caccia, C., Carotti, A., Salvati, P., Edmondson, D. E., and Mattevi, A. (2007) Structures of human monoamine oxidase B complexes with selective noncovalent inhibitors: Safinamide and coumarin analogs J. Med. Chem. 50, 5848-5852 (Pubitemid 350106038)
8. Binda, C., Newton-Vinson, P., Hubálek, F., Edmondson, D. E., and Mattevi, A. (2002) Structure of human monoamine oxidase B, a drug target for the treatment of neurological disorders Nat. Struct. Biol. 9, 22-26 (Pubitemid 34049174)
9. Edmondson, D. E., Binda, C., and Mattevi, A. (2004) The FAD binding sites of human monoamine oxidases A and B Neurotoxicology 25, 63-72 (Pubitemid 38044169)
10. Edmondson, D. E., Binda, C., and Mattevi, A. (2007) Structural insights into the mechanism of amine oxidation by monoamine oxidases A and B Arch. Biochem. Biophys. 464, 269-276 (Pubitemid 47210935)
11. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank Nucleic Acids Res. 28, 235-242 (Pubitemid 30047768)
12. Tsugeno, Y. and Ito, A. (1997) A Key amino acid responsible for substrate selectivity of monoamine oxidase A and B J. Biol. Chem. 272, 14033-14036 (Pubitemid 27232802)
13. Hubálek, F., Binda, C., Khalil, A., Li, M., Mattevi, A., Castagnoli, N., and Edmondson, D. E. (2005) Demonstration of isoleucine 199 as a structural determinant for the selective inhibition of human monoamine oxidase B by specific reversible inhibitors J. Biol. Chem. 280, 15761-15766 (Pubitemid 40616695)
14. Geha, R. M., Rebrin, I., Chen, K., and Shih, J. C. (2001) Substrate and inhibitor specificities for human monoamine oxidase A and B are influenced by a single amino acid J. Biol. Chem. 276, 9877-9882
15. Li, M., Binda, C., Mattevi, A., and Edmondson, D. E. (2006) Functional role of the aromatic cage in human monoamine oxidase B: Structures and catalytic properties of Tyr435 mutant proteins Biochemistry 45, 4775-4784
16. Fowler, P. W., Balali-Mood, K., Deol, S., Coveney, P. V., and Sansom, M. S. P. (2007) Monotopic enzymes and lipid bilayers: A Comparative Study Biochemistry 46, 3108-3115 (Pubitemid 46449133)
17. Apostolov, R., Yonezawa, Y., Standley, D. M., Kikugawa, G., Takano, Y., and Nakamura, H. (2009) Membrane attachment facilitates ligand access to the active site in monoamine oxidase A Biochemistry 48, 5864-5873
18. Binda, C., Li, M., Hubálek, F., Restelli, N., Edmondson, D. E., and Mattevi, A. (2003) Insights into the mode of inhibition of human mitochondrial monoamine oxidase B from high-resolution crystal structures Proc. Natl. Acad. Sci. U. S. A. 100, 9750-9755 (Pubitemid 37087013)
19. Binda, C., Hubálek, F., Li, M., Herzig, Y., Sterling, J., Edmondson, D. E., and Mattevi, A. (2005) Binding of rasagiline-related inhibitors to human monoamine oxidases: A kinetic and crystallographic analysis J. Med. Chem. 48, 8148-8154 (Pubitemid 43032523)
20. Case, D. A., Darden, T. A., Cheatham, III, T. E., Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Crowley, M., Walker, R. C., Zhang, W., Merz, K. M., Wang, B., Hayik, S., Roitberg, A., Seabra, G., Kolossvery, I., Wong, K. F., Paesani, F., Vanicek, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Yang, L., Tan, C., Mongan, J., Hornak, V., Cui, G., Mathews, D. H., Seetin, M. G., Sagui, C., Babin, V., and Kollman, P. A. (2008) AMBER 10, University of California, San Francisco, CA.
21. Schüttelkopf, A. W. and van Aalten, D. M. F. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D60, 1355-1363 (Pubitemid 41079731)
22. Lemkul, J. A., Allen, W. J., and Bevan, D. R. (2010) Practical considerations for building GROMOS-compatible small molecule topologies J. Chem. Inf. Model. 50, 2221-2235
23. Chirlian, L. E. and Francl, M. M. (1987) Atomic charges derived from electrostatic potentials: A detailed study J. Comput. Chem. 8, 894-905
24. Berger, O., Edholm, O., and Jähnig, F. (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72, 2002-2013 (Pubitemid 27184429)
25. Tieleman, D. P., Sansom, M. S. P., and Berendsen, H. J. C. (1999) Alamethicin helices in a bilayer and in solution: Molecular dynamics simulations Biophys. J. 76, 40-49 (Pubitemid 29202436)
26. van Meer, G., Voelker, D. R., and Feigenson, G. W. (2008) Membrane lipids: Where they are and how they behave Nat. Rev. Mol. Cell Biol. 9, 112-124 (Pubitemid 351158912)
27. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4, 435-447
28. Darden, T., York, D., and Pedersen, L. G. (1993) Particle mesh Ewald: An N-log(N) method for Ewald sums in large systems J. Chem. Phys. 98, 10089-10092
29. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald method J. Chem. Phys. 103, 8577-8593
30. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18, 1463-1472 (Pubitemid 127637344)
31. Hess, B. (2007) P-LINCS: A parallel linear constraint solver for molecular simulation J. Chem. Theory Comput. 4, 116-122
32. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., and Hermans, J. (1981) Intermolecular Forces, Interaction Models for Water in Relation to Protein Hydration, D. Reidel Publishing Co., Dordrecht, The Netherlands.
33. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath J. Chem. Phys. 81, 3684-3690
34. Nosé, S. (1984) A molecular dynamics method for simulations in the canonical ensemble Mol. Phys. 52, 255-268
35. Hoover, W. G. (1985) Canonical dynamics: Equilibrium phase-space distributions Phys. Rev. A 31, 1695-1697
36. Parrinello, M. and Rahman, A. (1981) Polymorphic transitions in single crystals: A new molecular dynamics method J. Appl. Phys. 52, 7182-7190 (Pubitemid 12456820)
37. Nosé, S. and Klein, M. L. (1983) Constant pressure molecular dynamics for molecular systems Mol. Phys. 50, 1055-1076
38. Kandt, C., Ash, W. L., and Tieleman, D. P. (2007) Setting up and running molecular dynamics simulations of membrane protiens Methods 41, 475-488 (Pubitemid 46400527)
39. DeLano, W. L. (2002) The PyMOL Users Manual, DeLano Scientific, Palo Alto, CA.
40. Turner, P. J. (2002) Grace, Center for Coastal and Land-Margin Research Oregon Graduate Institute of Science and Technology, Beaverton, OR.
41. Allen, W. J., Lemkul, J. A., and Bevan, D. R. (2009) GridMAT-MD: A grid based membrane analysis tool for use with molecular dynamics J. Comput. Chem. 30, 1952-1958
42. Kucìerka, N., Tristram-Nagle, S., and Nagle, J. F. (2005) Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains J. Membr. Biol. 208, 193-202
43. Rand, R. P., Fuller, N., Parsegian, V. A., and Rau, D. C. (1998) Variation in hydration forces between neutral phospholipid bilayers: Evidence for hydration attraction Biochemistry 27, 7711-7722
44. Hall, S. E., Roberts, K., and Vaidehi, N. (2009) Position of helical kinks in membrane protein crystal structures and the accuracy of computational prediction J. Mol. Graph. Model. 27, 944-950
45. Edmondson, D. E., Binda, C., Wang, J., Upadhyay, A. K., and Mattevi, A. (2009) Molecular and mechanistic properties of the membrane-bound mitochondrial monoamine oxidases Biochemistry 48, 4220-4230
46. Jarzynski, C. (1997) Nonequilibrium equality for free energy differences Phys. Rev. Lett. 78, 2690-2693 (Pubitemid 127655287)
47. Hubálek, F., Binda, C., Li, M., Herzig, Y., Sterling, J., Youdim, M. B. H., Mattevi, A., and Edmondson, D. E. (2004) Inactivation of purified human recombinant monoamine oxidases A and B by rasagiline and its analogues J. Med. Chem. 47, 1760-1766 (Pubitemid 38380919)
48. Sterling, J., Veinberg, A., Lerner, D., Goldenberg, W., Levy, R., Youdim, M., and Finberg, J. (1998) R)(+)-N-propargyl-1-aminoindan (rasagiline) and derviatives: highly selective and potent inhibitors of monoamine oxidase B J. Neural. Transm. 52, 301-305
49. Sterling, J., Herzig, Y., Goren, T., Finkelstein, N., Lerner, D., Goldenberg, W., Miskolczi, I., Molnar, S., Rantal, F., Tamas, T., Toth, G., Zagyva, A., Zekany, A., Lavian, G., Gross, A., Friedman, R., Razin, M., Huang, W., Krais, B., Chorev, M., Youdim, M. B., and Weinstock, M. (2002) Novel dual inhibitors of AChE and MAO derived from hydroxy aminoindan and phenethylamine as potential treatment for Alzheimers disease J. Med. Chem. 45, 5260-5279 (Pubitemid 35429165)
50. Colizzi, F., Perozzo, R., Scapozza, L., Recanatini, M., and Cavalli, A. (2010) Single-molecule pulling simulations can discern active from inactive enzyme inhibitors J. Am. Chem. Soc. 132, 7361-7371
51. Jorgensen, W. L. (2010) Drug discovery: Pulled from a proteins embrace Nature 466, 42-43
52. Baştuĝ, T., Chen, P.-C., Patra, S. M., and Kuyucak, S. (2008) Potential of mean force calculations of ligand binding to ion channels from Jarzynskis equality and umbrella sampling J. Chem. Phys. 128, 155104.155101-155104.155109