Influence of the environment on the oxidative deamination of p-substituted benzylamines in monoamine oxidase

Journal of Physical Chemistry B

Volumn 119, Issue 9, 2015, Pages 3678-3686

  Zenn, Roland K ^a   Abad, Enrique ^a,b   Kästner, Johannes ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

^b German Research School for Simulation Sciences   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; SUBSTRATES;

COMPUTATIONAL ANALYSIS; ELECTROSTATIC EFFECT; ENZYMATIC DECOMPOSITION; NUCLEOPHILIC MECHANISMS; OXIDATIVE DEAMINATION; RATE-LIMITING STEPS; REACTION MECHANISM; SUBSTITUTED BENZYLAMINES;

AMINES;

AMINE OXIDASE (FLAVIN CONTAINING); BENZYLAMINE DERIVATIVE;

CHEMISTRY; DEAMINATION; HUMAN; METABOLISM; MOLECULAR DYNAMICS; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; QUANTUM THEORY;

BENZYLAMINES; DEAMINATION; HUMANS; MOLECULAR DYNAMICS SIMULATION; MONOAMINE OXIDASE; OXIDATION-REDUCTION; PROTEIN CONFORMATION; QUANTUM THEORY;

EID: 84924055355     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp512470a     Document Type: Article

References (69)

1. Edmondson, D. E.; Binda, C.; Wang, J.; Upadhyay, A. K.; Mattevi, A. Molecular and Mechanistic Properties of the Membrane-Bound Mitochondrial Monoamine Oxidases Biochemistry 2009, 48, 4220-4230
2. Bach, A. W.; Lan, N. C.; Johnson, D. L.; Abell, C. W.; Bembenek, M. E.; Kwan, S. W.; Seeburg, P. H.; Shih, J. C. cDNA Cloning Of Human Liver Monoamine Oxidase A And B: Molecular Basis of Differences in Enzymatic Properties Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 4934-4938
3. Youdim, M. B. H.; Finberg, J. P. M.; Tipton, K. F. In Catecholamines; Trendelenburg, I.; Weiner, U., Eds.; Springer-Verlag: Berlin, 1988; pp 119-192.
4. Finberg, J. P. M. Update on the Pharmacology Of Selective Inhibitors Of MAO-A And MAO-B: Focus on Modulation Of CNS Monoamine Neurotransmitter Release Pharmacol. Ther. 2014, 143, 133-152
5. De Colibus, L.; Li, M.; Binda, C.; Lustig, A.; Edmondson, D. E.; Mattevi, A. Three-Dimensional Structure of Human Monoamine Oxidase A (MAO A): Relation to the Structures of Rat MAO A and Human MAO B Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 12684-12689
6. Zeller, E.; Barsky, J. In Vivo Inhibition of Liver and Brain Monoamine Oxidase By 1-Isonicotinyl-2-Isopropyl Hydrazine Proc. Soc. Exp. Biol. Med. 1952, 81, 459-461
7. Quitkin, F.; Rifkin, A.; Klein, D. F. Monoamine Oxidase Inhibitors. A Review of Antidepressant Effectiveness Arch. Gen. Psychiatry 1979, 36, 749-760
8. Zimmer, R. Relationship Between Tyramine Potentiation and Monoamine Oxidase (MAO) Inhibition: Comparison Between Moclobemide and Other MAO Inhibitors Acta Psychiatr. Scand. 1990, 82, 81-83
9. Kumar, M. J.; Nicholls, D. G.; Andersen, J. K. Oxidative Alpha-Ketoglutarate Dehydrogenase Inhibition Via Subtle Elevations in Monoamine Oxidase B Levels Results in Loss of Spare Respiratory Capacity: Implications for Parkinsons Disease J. Biol. Chem. 2003, 278, 46432-46439
10. Mallajosyula, J. K.; Kaur, D.; Chinta, S. J.; Rajagopalan, S.; Rane, A.; Nicholls, D. G.; Di Monte, D. A.; Macarthur, H.; Andersen, J. K. MAO-B Elevation in Mouse Brain Astrocytes Results in Parkinsons Pathology PLoS One 2008, 3, e1616
11. Searchword: monoamine oxidase. 2014; https://scifinder.cas.org.
12. Husain, M.; Edmondson, D. E.; Singer, T. P. Kinetic Studies on the Catalytic Mechanism of Liver Monoamine Oxidase Biochemistry 1982, 21, 595-600
13. Ramsay, R. R. Kinetic Mechanism of Monoamine Oxidase A Biochemistry 1991, 30, 4624-4629
14. Binda, C.; Newton-Vinson, P.; Hubálek, F.; Edmondson, D. E.; Mattevi, A. Structure of Human Monoamine Oxidase B, A Drug Target for the Treatment of Neurological Disorders Nat. Struct. Biol. 2002, 9, 22-26
15. Binda, C.; Li, M.; Hubalek, F.; Restelli, N.; Edmondson, D. E.; Mattevi, A. Insights into the Mode of Inhibition of Human Mitochondrial Monoamine Oxidase B from High-Resolution Crystal Structures Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 9750-9755
16. Li, M.; Binda, C.; Mattevi, A.; Edmondson, D. E. Functional Role of the Aromatic Cage in Human Monoamine Oxidase B: Structures and Catalytic Properties of Tyr435 Mutant Proteins Biochemistry 2006, 45, 4775-4784
17. Belleau, B.; Fang, M.; Burba, J.; Moran, J. The Absolute Optical Specificity of Monoamine Oxidase J. Am. Chem. Soc. 1960, 82, 5752-5754
18. Yu, P. H.; Bailey, B. A.; Durden, D. A.; Boulton, A. A. Stereospecific Deuterium Substitution at the α-Carbon Position of Dopamine and its Effect on Oxidative Deamination Catalyzed by MAO-A and MAO-B from Different Tissues Biochem. Pharmacol. 1986, 35, 1027-1036
19. Miller, J. R.; Edmondson, D. E. Structure-Activity Relationships in the Oxidation of Para-Substituted Benzylamine Analogues by Recombinant Human Liver Monoamine Oxidase A Biochemistry 1999, 38, 13670-13683
20. Erdem, S. S.; Karahan, O.; Yildiz, I.; Yelekçi, K. A Computational Study on The Amine-Oxidation Mechanism of Monoamine Oxidase: Insight into the Polar Nucleophilic Mechanism Org. Biomol. Chem. 2006, 4, 646-658
21. MacMillar, S.; Edmondson, D. E.; Matsson, O. Nitrogen Kinetic Isotope Effects for the Monoamine Oxidase B-Catalyzed Oxidation of Benzylamine and (1,1-(2)H2)Benzylamine: Nitrogen Rehybridization And CH Bond Cleavage Are Not Concerted J. Am. Chem. Soc. 2011, 133, 12319-12321
22. Akyüz, M. A.; Erdem, S. S. Computational Modeling of the Direct Hydride Transfer Mechanism for the MAO Catalyzed Oxidation of Phenethylamine and Benzylamine: ONIOM (QM/QM) Calculations J. Neural Transm. 2013, 120, 937-945
23. Ralph, E. C.; Hirschi, J. S.; Anderson, M. A.; Cleland, W. W.; Singleton, D. A.; Fitzpatrick, P. F. Insights into the Mechanism of Flavoprotein-Catalyzed Amine Oxidation from Nitrogen Isotope Effects on the Reaction of N-Methyltryptophan Oxidase Biochemistry 2007, 46, 7655-7664
24. Fitzpatrick, P. F. Oxidation of Amines by Flavoproteins Arch. Biochem. Biophys. 2010, 493, 13-25
25. Vianello, R.; Repič, M.; Mavri, J. How are Biogenic Amines Metabolized by Monoamine Oxidases? Eur. J. Org. Chem. 2012, 2012, 7057-7065
26. Abad, E.; Zenn, R. K.; Kästner, J. Reaction Mechanism of Monoamine Oxidase from QM/MM Calculations J. Phys. Chem. B 2013, 117, 14238-14246
27. Kurtz, K. A.; Rishavy, M. A.; Cleland, W. W.; Fitzpatrick, P. F. Nitrogen Isotope Effects As Probes of the Mechanism of D-Amino Acid Oxidase J. Am. Chem. Soc. 2000, 122, 12896-12897
28. Lu, X.; Rodriguez, M.; Ji, H.; Silverman, R. B.; Vintem, A. P. B.; Ramsay, R. R. In Flavins and flavoproteins 2002; Chapman, S. K.; Perham, R. N.; Scrutton, N. S., Eds.; Rudolf Weber, Agency for Scientific Publications: Berlin, 2002.
29. Ramsay, R. R.; Upadhyay, A. K.; Li, M.; Edmondson, D. E. In Flavins and Flavoproteins; Nishino, T.; Miura, R.; Fukui, K.; Tanokura, M., Eds.; ArchiTect, Inc.: Tokio, 2005; pp 137-142.
30. Edmondson, D. E.; Binda, C.; Mattevi, A. Structural Insights into the Mechanism of Amine Oxidation by Monoamine Oxidases A and B Arch. Biochem. Biophys. 2007, 464, 269-276
31. Erdem, S. S.; Büyükmenekşe, B. Computational Investigation on the Structure-Activity Relationship of the Biradical Mechanism for Monoamine Oxidase J. Neural Transm. 2011, 118, 1021-1029
32. Hamilton, G. A.; Brown, L. E. Model Reactions and a General Mechanism for Flavoenzyme-Catalyzed Dehydrogenations J. Am. Chem. Soc. 1970, 92, 7225-7227
33. Kim, J. M.; Bogdan, M. A.; Mariano, P. S. Mechanistic Analysis Of The 3-Methyllumiflavin-Promoted Oxidative Deamination Of Benzylamine. A Potential Model For Monoamine Oxidase Catalysis J. Am. Chem. Soc. 1993, 115, 10591-10595
34. Newton-Vinson, P.; Hubalek, F.; Edmondson, D. E. High-Level Expression of Human Liver Monoamine Oxidase B in Pichia Pastoris Protein Expression Purif. 2000, 20, 334-345
35. Jonsson, T.; Edmondson, D. E.; Klinman, J. P. Hydrogen Tunneling in the Flavoenzyme Monoamine Oxidase B Biochemistry 1994, 33, 14871-14878
36. Akyüz, M. A.; Erdem, S. S.; Edmondson, D. E. The Aromatic Cage in the Active Site of Monoamine Oxidase B: Effect on the Structural and Electronic Properties of Bound Benzylamine and p-Nitrobenzylamine J. Neural Transm. 2007, 114, 693-698
37. Repič, M.; Vianello, R.; Purg, M.; Duarte, F.; Bauer, P.; Kamerlin, S. C. L.; Mavri, J. Empirical Valence Bond Simulations of the Hydride Transfer Step in the Monoamine Oxidase B Catalyzed Metabolism of Dopamine Proteins 2014, 82, 3347-3355
38. Cooper, A. M.; Kästner, J. Averaging Techniques for Reaction Barriers in QM/MM Simulations ChemPhysChem 2014, 15, 3264-3269
39. ChemShell, version 3.6.dev; a Computational Chemistry Shell; see STFC Daresbury Laboratory UK, 2014.
40. Metz, S.; Kästner, J.; Sokol, A. A.; Keal, T. W.; Sherwood, P. ChemShell-A Modular Software Package for QM/MM Simulations Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2014, 4, 101-110
41. Kästner, J.; Carr, J. M.; Keal, T. W.; Thiel, W. Wander, A.; Sherwood, P. DL-FIND: an Open-Source Geometry Optimizer for Atomistic Simulations J. Phys. Chem. A 2009, 113, 11856-11865
42. Becke, A. D. Density-Functional Exchange-Energy Approximation with Correct Asymptotic Behavior Phys. Rev. A 1988, 38, 3098-3100
43. Perdew, J. Density-Functional Approximation for the Correlation Energy of the Inhomogeneous Electron Gas Phys. Rev. B 1986, 33, 8822-8824
44. Weigend, F.; Häser, M.; Patzelt, H.; Ahlrichs, R. RI-MP2: Optimized Auxiliary Basis Sets and Demonstration of Efficiency Chem. Phys. Lett. 1998, 294, 143-152
45. Weigend, F.; Ahlrichs, R. Balanced Basis Sets of Split Valence, Triple Zeta Valence and Quadruple Zeta Valence Quality for H to Rn: Design and Assessment of Accuracy Phys. Chem. Chem. Phys. 2005, 7, 3297-3305
46. TURBOMOLE, V6.3; a development of University of Karlsruhe and Forschungszentrum Karlsruhe GmbH, 1989-2007, TURBOMOLE GmbH, since 2007 available from http://www.turbomole.com; Karlsruhe, Germany, 2011.
47. Rommel, J. B.; Kästner, J. The Fragmentation-Recombination Mechanism of the Enzyme Glutamate Mutase Studied by QM/MM Simulations J. Am. Chem. Soc. 2011, 133, 10195-10203
48. Henkelman, G.; Jónsson, H. A Dimer Method for Finding Saddle Points on High Dimensional Potential Surfaces Using Only First Derivatives J. Chem. Phys. 1999, 111, 7010-7022
49. Kästner, J.; Sherwood, P. Superlinearly Converging Dimer Method for Transition State Search J. Chem. Phys. 2008, 128, 014106
50. Zhao, Y.; Truhlar, D. G. A New Local Density Functional for Main-Group Thermochemistry, Transition Metal Bonding, Thermochemical Kinetics, and Noncovalent Interactions J. Chem. Phys. 2006, 125, 194101
51. Werner, H.-J.; Knowles, P. J.; Manby, F. R.; Schütz, M.; Celani, P.; Knizia, G.; Korona, T.; Lindh, R.; Mitrushenkov, A.; Rauhut, G.; MOLPRO, development version, a package of ab initio programs (see www.molpro.net); University College Cardiff Consultants Limited: Cardiff, U.K., 2014.
52. Rommel, J. B.; Liu, Y.; Werner, H.-J.; Kästner, J. Role of Tunneling in the Enzyme Glutamate Mutase J. Phys. Chem. B 2012, 116, 13682-13689
53. Reed, A. E.; Curtiss, L. A.; Weinhold, F. Intermolecular Interactions From A Natural Bond Orbital, Donor-Acceptor Viewpoint Chem. Rev. 1988, 88, 899-926
54. Knizia, G. Intrinsic Atomic Orbitals: An Unbiased Bridge between Quantum Theory and Chemical Concepts J. Chem. Theory Comput. 2013, 9, 4834-4843
55. Mackerell, A. D.; Feig, M.; Brooks, C. L. Extending the Treatment of Backbone Energetics in Protein Force Fields: Limitations of Gas-Phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations J. Comput. Chem. 2004, 25, 1400-1415
56. MacKerell, A. D.; MacKerell, A. D.; Bashford, D.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
57. Feller, S. E.; Gawrisch, K.; MacKerell, A. D. Polyunsaturated Fatty Acids in Lipid Bilayers: Intrinsic and Environmental Contributions to their Unique Physical Properties J. Am. Chem. Soc. 2002, 124, 318-326
58. Feller, S. E.; MacKerell, A. D. An Improved Empirical Potential Energy Function for Molecular Simulations of Phospholipids J. Phys. Chem. B 2000, 104, 7510-7515
59. Schlenkrich, M.; Brickmann, J.; MacKerell, A., Jr.; Karplus, M. In Biological Membranes: A Molecular Perspective from Computation and Experiment; Merz, K. M.; Roux, B., Eds.; Birkhauser Boston Inc: Boston, MA, 1996; pp 31-81.
60. Foloppe, N.; MacKerell, A. D., Jr. All-atom Empirical Force Field for Nucleic Acids: I. Parameter Optimization Based on Small Molecule and Condensed Phase Macromolecular Target Data J. Comput. Chem. 2000, 21, 86-104
61. MacKerell, A. D.; Banavali, N. K. All-atom Empirical Force Field for Nucleic Acids II. Application to Molecular Dynamics Simulations of DNA And RNA in Solution J. Comput. Chem. 2000, 21, 105-120
62. Smith, W.; Yong, C.; Rodger, P. DL-POLY: Application to Molecular Simulation Mol. Simul. 2002, 28, 385-471
63. Eckart, C. The Penetration of a Potential Barrier by Electrons Phys. Rev. 1930, 35, 1303-1309
64. Son, S.-Y.; Ma, J.; Kondou, Y.; Yoshimura, M.; Yamashita, E.; Tsukihara, T. Structure of Human Monoamine Oxidase A at 2.2-Å Resolution: The Control of Opening the Entry for Substrates/Inhibitors Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 5739-5744
65. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kalé, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
66. Orru, R.; Aldeco, M.; Edmondson, D. E. Do MAO A and MAO B Utilize The Same Mechanism for the C-H Bond Cleavage Step in Catalysis? Evidence Suggesting Differing Mechanisms J. Neural Transm. 2013, 120, 847-851
67. Molla, G.; Nardini, M.; Motta, P.; DArrigo, P.; Panzeri, W.; Pollegioni, L. Aminoacetone Oxidase from Streptococcus Oligofermentas Belongs to a New Three-Domain Family of Bacterial Flavoproteins Biochem. J. 2014, 464, 387-399
68. Ferreira, P.; Villanueva, R.; Martínez-Júlvez, M.; Herguedas, B.; Marcuello, C.; Fernandez-Silva, P.; Cabon, L.; Hermoso, J. A.; Lostao, A.; Susin, S. A. Structural Insights into the Coenzyme Mediated Monomer-Dimer Transition of the Pro-Apoptotic Apoptosis Inducing Factor Biochemistry 2014, 53, 4204-4215
69. Walker, M. C.; Edmondson, D. E. Structure-Activity Relationships in the Oxidation of Benzylamine Analogues by Bovine Liver Mitochondrial Monoamine Oxidase B Biochemistry 1994, 33, 7088-7098