Conformational behavior of flavin adenine dinucleotide: Conserved stereochemistry in bound and free states

Journal of Physical Chemistry B

Volumn 118, Issue 47, 2014, Pages 13486-13497

  Kuppuraj, Gopi ^a   Kruise, Dennis ^a,c   Yura, Kei ^a,b  

^a OCHANOMIZU UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c HANZE UNIVERSITY OF APPLIED SCIENCES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; ENZYMES; MOLECULAR DYNAMICS; MOLECULES; NUCLEOTIDES; PRINCIPAL COMPONENT ANALYSIS; REACTION KINETICS; X RAY CRYSTALLOGRAPHY;

ADENOSINE MONOPHOSPHATE; BIOCHEMICAL REACTIONS; CONFORMATIONAL BEHAVIOR; CONFORMATIONAL DYNAMICS; CRYSTALLOGRAPHIC DATA; ENZYMATIC ACTIVITIES; FLAVIN ADENINE DINUCLEOTIDE; MOLECULAR DYNAMICS SIMULATIONS;

DIHEDRAL ANGLE;

1,5-DIHYDRO-FAD; FLAVINE ADENINE NUCLEOTIDE; ION; WATER;

ANALOGS AND DERIVATIVES; CHEMICAL STRUCTURE; CHEMISTRY; MOLECULAR DYNAMICS; OXIDATION REDUCTION REACTION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; FLAVIN-ADENINE DINUCLEOTIDE; IONS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; WATER;

EID: 84913557557     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp507629n     Document Type: Conference Paper

References (68)

1. Dym, O.; Eisenberg, D. Sequence-Structure Analysis of FAD-Containing Proteins. Protein Sci. 2001, 10 (9), 1712-1728.
2. Solov'yov, I. A.; Domratcheva, T.; Moughal Shahi, A. R.; Schulten, K. Decrypting Cryptochrome: Revealing The Molecular Identity of the Photoactivation Reaction. J. Am. Chem. Soc. 2012, 134 (43), 18046-18052.
3. Solov'yov, I. A.; Domratcheva, T.; Schulten, K. Separation of Photo-Induced Radical Pair in Cryptochrome to a Functionally Critical Distance. Sci. Rep. 2014, 4 (3485), 1-8.
4. Miyazawa, Y.; Nishioka, H.; Yura, K.; Yamato, T. Discrimination of Class I Cyclobutane Pyrimidine Dimer Photolyase from Blue Light Photoreceptors by Single Methionine Residue. Biophys. J. 2008, 94 (6), 2194-2203.
5. Kao, Y.-T.; Saxena, C.; Wang, L.; Sancar, A.; Zhong, D. Direct Observation of Thymine Dimer Repair in DNA by Photolyase. Proc. Natl. Acad. Sci. U. S. A. 2005, 102 (45), 16128-16132.
6. Mees, A.; Klar, T.; Gnau, P.; Hennecke, U.; Eker, A. P. M.; Carell, T.; Essen, L.-O. Crystal Structure of a Photolyase Bound to A CPD-Like DNA Lesion After In Situ Repair. Science 2004, 306 (5702), 1789-1793.
7. Sancar, A. Structure And Function of DNA Photolyase And Cryptochrome Blue-Light Photoreceptors. Chem. Rev. 2003, 103 (6), 2203-2238.
8. Thiagarajan, V.; Villette, S.; Espagne, A.; Eker, A. P. M.; Brettel, K.; Byrdin, M. DNA Repair by Photolyase: A Novel Substrate with Low Background Absorption around 265 nm for Transient Absorption Studies in the UV. Biochemistry 2009, 49 (2), 297-303.
9. Weber, S. Light-Driven Enzymatic Catalysis of DNA Repair: A Review of Recent Biophysical Studies on Photolyase. Bioenergetics 2005, 1707 (1), 1-23.
10. Ai, Y.-J.; Zhang, F.; Chen, S.-F.; Luo, Y.; Fang, W.-H. Importance of the Intramolecular Hydrogen Bond on the Photochemistry of Anionic Hydroquinone (FADH-) in DNA Photolyase. J. Phys. Chem. Lett. 2010, 1 (4), 743-747.
11. Hahn, J.; Michel-Beyerle, M.-E.; Rösch, N. Conformation of The Flavin Adenine Dinucleotide Cofactor FAD in DNA-Photolyase: A Molecular Dynamics Study. J. Mol. Model. 1998, 4 (2), 73-82.
12. Henriques, B. J.; Rodrigues, J. V.; Olsen, R. K.; Bross, P.; Gomes, C. M. Role of Flavinylation in a Mild Variant of Multiple Acyl-CoA Dehydrogenation Deficiency: A Molecular Rationale for the Effects of Riboflavin Supplementation. J. Biol. Chem. 2009, 284 (7), 4222-4229.
13. Kim, H. J.; Jeong, M.-Y.; Na, U.; Winge, D. R. Flavinylation and Assembly of Succinate Dehydrogenase are Dependent on the C-Terminal Tail of the Flavoprotein Subunit. J. Biol. Chem. 2012, 287 (48), 40670-40679.
14. Kim, H. J.; Winge, D. R. Emerging Concepts in the Flavinylation of Succinate Dehydrogenase. Bioenergetics 2013, 1827 (5), 627-636.
15. Kopacz, M. M.; Rovida, S.; Van Duijn, E.; Fraaije, M. W.; Mattevi, A. Structure-Based Redesign of Cofactor Binding in Putrescine Oxidase. Biochemistry 2011, 50 (19), 4209-4217.
16. Krysiak, J. M.; Kreuzer, J.; Macheroux, P.; Hermetter, A.; Sieber, S. A.; Breinbauer, R. Activity-Based Probes for Studying the Activity of Flavin-Dependent Oxidases and for the Protein Target Profiling of Monoamine Oxidase Inhibitors. Angew. Chem., Int. Ed. 2012, 51 (28), 7035-7040.
17. Long, Q.; Ji, L.; Wang, H.; Xie, J. Riboflavin Biosynthetic and Regulatory Factors as Potential Novel Anti-Infective Drug Targets. Chem. Biol. Drug Des. 2010, 75 (4), 339-347.
18. Lucas, T. G.; Henriques, B. J.; Rodrigues, J. V.; Bross, P.; Gregersen, N.; Gomes, C. M. Cofactors and Metabolites as Potential Stabilizers of Mitochondrial Acyl-CoA Dehydrogenases. Biochim Biophys Acta 2011, 1812 (12), 1658-1663.
19. Mansoorabadi, S. O.; Thibodeaux, C. J.; Liu, H.-W. The Diverse Roles of Flavin Coenzymes: Nature's Most Versatile Thespians. J. Org. Chem. 2007, 72 (17), 6329-6342.
20. Van Maldegem, B. T.; Duran, M.; Wanders, R. J. A.; Waterham, H. R.; Wijburg, F. A. Flavin Adenine Dinucleotide Status and the Effects of High-Dose Riboflavin Treatment in Short-Chain Acyl-CoA Dehydrogenase Deficiency. Pediatr. Res. 2010, 67 (3), 304-308.
21. Bostroem, J. Reproducing the Conformations of Protein-Bound Ligands: A Critical Evaluation of Several Popular Conformational Searching Tools. J. Comput.-Aided Mol. Des. 2001, 15 (12), 1137-1152.
22. Butler, K. T.; Luque, F. J.; Barril, X. Toward Accurate Relative Energy Predictions of the Bioactive Conformation of Drugs. J. Comput. Chem. 2009, 30 (4), 601-610.
23. Moodie, S. L.; Thornton, J. M. A Study into the Effects of Protein Binding on Nucleotide Conformation. Nucleic Acids Res. 1993, 21 (6), 1369-1380.
24. Nicklaus, M. C.; Wang, S.; Driscoll, J. S.; Milne, G. W. A. Conformational Changes of Small Molecules Binding to Proteins. Bioorg. Med. Chem. 1995, 3 (4), 411-428.
25. Perola, E.; Charifson, P. S. Conformational Analysis of Drug-Like Molecules Bound to Proteins: An Extensive Study of Ligand Reorganization upon Binding. J. Med. Chem. 2004, 47 (10), 2499-2510.
26. Stockwell, G. R.; Thornton, J. M. Conformational Diversity of Ligands Bound to Proteins. J. Mol. Biol. 2006, 356 (4), 928-944.
27. Bell, C. E.; Yeates, T. O.; Eisenberg, D. Unusual Conformation of Nicotinamide Adenine Dinucleotide (NAD) Bound to Diphtheria Toxin: A Comparison with NAD Bound to the Oxidoreductase Enzymes. Protein Sci. 1997, 6 (10), 2084-2096.
28. Kuppuraj, G.; Sargsyan, K.; Hua, Y.-H.; Merrill, A. R.; Lim, C. Linking Distinct Conformations of Nicotinamide Adenine Dinucleotide with Protein Fold/Function. J. Phys. Chem. B 2011, 115 (24), 7932-7939.
29. Fischer, J. D.; Holliday, G. L.; Rahman, S. A.; Thornton, J. M. The Structures and Physicochemical Properties of Organic Cofactors in Biocatalysis. J. Mol. Biol. 2010, 403 (5), 803-824.
30. Fischer, J. D.; Holliday, G. L.; Thornton, J. M. The Cofactor Database: Organic Cofactors in Enzyme Catalysis. Bioinformatics 2010, 26 (19), 2496-2497.
31. Holliday, G. L.; Fischer, J. D.; Mitchell, J. B. O.; Thornton, J. M. Characterizing The Complexity of Enzymes on the Basis of their Mechanisms and Structures with a Bio-Computational Analysis. FEBS J. 2011, 278 (20), 3835-3845.
32. Stegemann, B.; Klebe, G. Cofactor-Binding Sites in Proteins of Deviating Sequence: Comparative Analysis and Clustering in Torsion Angle, Cavity, and Fold Space. Proteins: Struct., Funct., Bioinf. 2012, 80 (2), 626-648.
33. Djordjevic, S.; Pace, C. P.; Stankovich, M. T.; Kim, J.-J. P. Three-Dimensional Structure of Butyryl-CoA Dehydrogenase from Megasphaera Elsdenii. Biochemistry 1995, 34 (7), 2163-2171.
34. Lantwin, C. B.; Schlichting, I.; Kabsch, W.; Pai, E. F.; Krauth-Siegel, R. L. The Structure of Trypanosoma Cruzitrypanothione Reductase in the Oxidized and NADPH Reduced State. Proteins: Struct., Funct., Bioinf. 1994, 18 (2), 161-173.
35. Mattevi, A.; Obmolova, G.; Kalk, K. H.; Van Berkel, W. J. H.; Hol, W. G. J. Three-Dimensional Structure of Lipoamide Dehydrogenase from Pseudomonas Fluorescens At 2 Σ 8 ≈ Resolution: Analysis of Redox and Thermostability Properties. J. Mol. Biol. 1993, 230 (4), 1200-1215.
36. Mittl, P. R. E.; Schulz, G. E. Structure of Glutathione Reductase from Escherichia Coli at 1.86 A˚ Resolution: Comparison with the Enzyme from Human Erythrocytes. Protein Sci. 1994, 3 (5), 799-809.
37. Waksman, G.; Krishna, T. S. R.; Williams, C. H.; Kuriyan, J. Crystal Structure Of Escherichia Coli Thioredoxin Reductase Refined at 2 A˚ Resolution: Implication for a Large Conformational Change during Catalysis. J. Mol. Biol. 1994, 236 (3), 800-816.
38. Grininger, M.; Seiler, F.; Zeth, K.; Oesterhelt, D. Dodecin Sequesters FAD in Closed Conformation from The Aqueous Solution. J. Mol. Biol. 2006, 364 (4), 561-566.
39. Van Den Berg, P. A. W.; Feenstra, K. A.; Mark, A. E.; Berendsen, H. J. C.; Visser, A. J. W. G. Dynamic Conformations Of Flavin Adenine Dinucleotide:,Äâ Simulated Molecular Dynamics Of The Flavin Cofactor Related To The Time-Resolved Fluorescence Characteristics. J. Phys. Chem. B 2002, 106 (34), 8858-8869.
40. Radoszkowicz, L.; Huppert, D.; Nachliel, E.; Gutman, M. Sampling the Conformation Space of FAD in Water-Methanol Mixtures through Molecular Dynamics and Fluorescence Measurements. J. Phys. Chem. A 2009, 114 (2), 1017-1022.
41. Brakoulias, A.; Jackson, R. M. Towards a Structural Classification of Phosphate Binding Sites in Protein - Nucleotide Complexes: An Automated All-Against-All Structural Comparison Using Geometric Matching. Proteins: Struct., Funct., Bioinf. 2004, 56 (2), 250-260.
42. Er, T.-K.; Chen, C.-C.; Liu, Y.-Y.; Chang, H.-C.; Chien, Y.-H.; Chang, J.-G.; Hwang, J.-K.; Jong, Y.-J. Computational Analysis of a Novel Mutation in ETFDH Gene Highlights its Long-Range Effects on the FAD-Binding Motif. BMC Struct. Biol. 2011, 11 (1), 43.
43. Gherardini, P. F.; Ausiello, G.; Russell, R. B.; Helmer-Citterich, M. Modular Architecture of Nucleotide-Binding Pockets. Nucleic Acids Res. 2010, 38 (11), 3809-3816.
44. Hirsch, A. K. H.; Fischer, F. R.; Diederich, F. Phosphate Recognition in Structural Biology. Angew. Chem., Int. Ed. 2007, 46 (3), 338-352.
45. Kinoshita, K.; Sadanami, K.; Kidera, A.; Go, N. Structural Motif of Phosphate-Binding Site Common to Various Protein Superfamilies: All-Against-All Structural Comparison of Protein-Mononucleotide Complexes. Protein Eng. 1999, 12 (1), 11-14.
46. Kleiger, G.; Eisenberg, D. GXXXG And GXXXA Motifs Stabilize FAD and NAD(P)-Binding Rossmann Folds through C[Alpha]-H⋯O Hydrogen Bonds and van Der Waals Interactions. J. Mol. Biol. 2002, 323 (1), 69-76.
47. Parca, L.; Gherardini, P. F.; Helmer-Citterich, M.; Ausiello, G. Phosphate Binding Sites Identification in Protein Structures. Nucleic Acids Res. 2011, 39 (4), 1231-1242.
48. Schulz, G. E. Binding of Nucleotides by Proteins. Curr. Opin. Struct. Biol. 1992, 2 (1), 61-67.
49. Feng, Z.; Chen, L.; Maddula, H.; Akcan, O.; Oughtred, R.; Berman, H. M.; Westbrook, J. Ligand Depot: A Data Warehouse for Ligands Bound to Macromolecules. Bioinformatics 2004, 20 (13), 2153-2155.
50. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank. Nucleic Acids Res. 2000, 28 (1), 235-242.
51. Sargsyan, K.; Wright, J.; Lim, C. Geopca: A New Tool For Multivariate Analysis of Dihedral Angles Based on Principal Component Geodesics. Nucleic Acids Res. 2012, 40 (3), E25.
52. Grant, B. J.; Rodrigues, A. P. C.; Elsawy, K. M.; Mccammon, J. A.; Caves, L. S. D. Bio3d: An R Package for the Comparative Analysis of Protein Structures. Bioinformatics 2006, 22 (21), 2695-2696.
53. Hess, B.; Kutzner, C.; Van Der Spoel, D.; Lindahl, E. Gromacs 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J. Chem. Theory Comput. 2008, 4 (3), 435-447.
54. Schuttelkopf, A. W.; Van Aalten, D. M. F. PRODRG: A Tool for High-Throughput Crystallography of Protein-Ligand Complexes. Acta Crystallogr., Sect. D 2004, 60 (8), 1355-1363.
55. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A Linear Constraint Solver for Molecular Simulations. J. Comput. Chem. 1997, 18 (12), 1463-1472.
56. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An N? Log(N) Method for Ewald Sums in Large Systems. J. Chem. Phys. 1993, 98 (12), 10089-10092.
57. Webb, L. E.; Hill, E. J.; Banaszak, L. J. Conformation of Nicotinamide Adenine Dinucleotide Bound to Cytoplasmic Malate Dehydrogenase. Biochemistry 1973, 12 (25), 5101-5109.
58. Denessiouk, K. A.; Johnson, M. S. When Fold Is Not Important: A Common Structural Framework for Adenine and AMP Binding in 12 Unrelated Protein Families. Proteins: Struct., Funct., Bioinf. 2000, 38 (3), 310-326.
59. Denessiouk, K. A.; Rantanen, V.-V.; Johnson, M. S. Adenine Recognition: A Motif Present in ATP-, CoA-, NAD-, NADP-, and FAD-Dependent Proteins. Proteins: Struct., Funct., Bioinf. 2001, 44 (3), 282-291.
60. Chosrowjan, H.; Taniguchi, S.; Mataga, N.; Tanaka, F.; Visser, A. J. W. G. The Stacked Flavin Adenine Dinucleotide Conformation in Water is Fluorescent on Picosecond Timescale. Chem. Phys. Lett. 2003, 378 (3-4), 354-358.
61. Nakabayashi, T.; Islam, M. S.; Ohta, N. Fluorescence Decay Dynamics of Flavin Adenine Dinucleotide in a Mixture of Alcohol and Water in the Femtosecond and Nanosecond Time Range. J. Phys. Chem. B 2010, 114 (46), 15254-15260.
62. Radoszkowicz, L.; Presiado, I.; Erez, Y.; Nachliel, E.; Huppert, D.; Gutman, M. Time-Resolved Emission of Flavin Adenine Dinucleotide in Water and Water-Methanol Mixtures. Phys. Chem. Chem. Phys. 2011, 13 (25), 12058-12066.
63. Sengupta, A.; Sasikala, W. D.; Mukherjee, A.; Hazra, P. Comparative Study of Flavins Binding with Human Serum Albumin: A Fluorometric, Thermodynamic, and Molecular Dynamics Approach. ChemPhysChem 2012, 13 (8), 2142-2153.
64. Sengupta, A.; Gavvala, K.; Koninti, R. K.; Chaudhuri, H.; Hazra, P. Folding Dynamics of Flavin Adenine Dinucleotide (FAD) Inside Non-Aqueous and Aqueous Reverse Micelles. Chem. Phys. Lett. 2013, 584 (0), 67-73.
65. Lemkul, J. A.; Allen, W. J.; Bevan, D. R. Practical Considerations for Building GROMOS-Compatible Small-Molecule Topologies. J. Chem. Inf. Model. 2010, 50 (12), 2221-2235.
66. Rao, S. T.; Rossmann, M. G. Comparison of Super-Secondary Structures in Proteins. J. Mol. Biol. 1973, 76 (2), 241-256.
67. Rossmann, M. G.; Liljas, A.; Branden, C. I.; Banaszak, L. T. Evolutionary and Structural Relationships among Dehydrogenases. Enzymes 1975, 11, 61-102.
68. Sengupta, A.; Singh, R. K.; Gavvala, K.; Koninti, R. K.; Mukherjee, A.; Hazra, P. Urea Induced Unfolding Dynamics of Flavin Adenine Dinucleotide (FAD): Spectroscopic and Molecular Dynamics Simulation Studies from Femto-Second to Nanosecond Regime. J. Phys. Chem. B 2014, 118 (7), 1881-1890.