Molecular dynamics simulations of heart-type fatty acid binding protein in apo and holo forms, and hydration structure analyses in the binding cavity

Journal of Physical Chemistry B

Volumn 119, Issue 1, 2015, Pages 114-127

  Matsuoka, Daisuke ^a   Sugiyama, Shigeru ^a   Murata, Michio ^a   Matsuoka, Shigeru ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HYDRATION; HYDROGEN BONDS; HYDROPHOBICITY; LIGANDS; MOLECULAR DYNAMICS; PROTEINS; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHIC STUDIES; HEART-TYPE FATTY ACID; HYDRATION STRUCTURE; HYDROGEN BOND NETWORKS; HYDROPHOBIC INTERACTIONS; LIPID-BINDING PROTEINS; MOLECULAR DYNAMICS SIMULATIONS; THREE-DIMENSIONAL STRUCTURE;

FATTY ACIDS;

APOPROTEIN; FABP3 PROTEIN, HUMAN; FATTY ACID BINDING PROTEIN; WATER;

BINDING SITE; CHEMISTRY; HEART MUSCLE; HUMAN; HYDROGEN BOND; MOLECULAR DYNAMICS; PROTEIN CONFORMATION;

APOPROTEINS; BINDING SITES; FATTY ACID-BINDING PROTEINS; HUMANS; HYDROGEN BONDING; MOLECULAR DYNAMICS SIMULATION; MYOCARDIUM; PROTEIN CONFORMATION; WATER;

EID: 84920713521     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp510384f     Document Type: Article

References (82)

1. Veerkamp, J. H.; Peeters, R. A.; Maatman, R. G. H. J. Structural and Functional Features of Different Types of Cytoplasmic Fatty Acid-Binding Proteins. Biochim. Biophys. Acta 1991, 1081, 1-24.
2. Banaszak, L.; Winter, N.; Xu, Z.; Bernlohr, D. A.; Cowan, S.; Jones, T. A. Lipid-Binding Proteins: a Family of Fatty Acid and Retinoid Transport Proteins. Adv. Protein Chem. 1994, 45, 89-151.
3. Glatz, J. F. C.; van der Vusse, G. J. Cellular Fatty Acid-Binding Proteins: Their Function and Physiological Significance. Prog. Lipid Res. 1996, 35, 243-282.
4. Hohoff, C.; Spener, F. Fatty Acid Binding Proteins and Mammary-Derived Growth Inhibitor. Fett/Lipid 1998, 100, 252-263.
5. Lücke, C.; Gutiérrez-González, L. H.; Hamilton, J. A. Intracellular Lipid Binding Proteins: Evolution, Structure, and Ligand Binding. In Cellular Proteins and their Fatty Acids in Health and Disease; Duttaroy, A. K., Spener, F., Eds.; Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, 2003; pp 95-118.
6. Haunerland, N. H.; Spener, F. Fatty Acid-Binding Proteins - Insights from Genetic Manipulations. Prog. Lipid Res. 2004, 43, 328-349.
7. Furuhashi, M.; Hotamisligil, G. S. Fatty Acid-Binding Proteins: Role in Metabolic Diseases and Potential as Drug Targets. Nat. Rev. Drug Discovery 2008, 7, 489-503.
8. Glatz, J. F. C.; Paulussen, R. J. A.; Veerkamp, J. H. Fatty Acid Binding Proteins from Heart. Chem. Phys. Lipids 1985, 38, 115-129.
9. Storch, J.; Thumser, A. E. A. The Fatty Acid Transport Function of Fatty Acid-Binding Proteins. Biochim. Biophys. Acta 2000, 1486, 28-44.
10. Hertzel, A. V.; Bernlohr, D. A. The Mammalian Fatty Acidbinding Protein Multigene Family: Molecular and Genetic Insights into Function. Trends Endocrin. Met. 2000, 11, 175-180.
11. Storch, J.; Thumser, A. E. Tissue-Specific Functions in the Fatty Acid-binding Protein Family. J. Biol. Chem. 2010, 285, 32679-32683.
12. Zanotti, G.; Scapin, G.; Spadon, P.; Veerkamp, J. H.; Sacchetttini, J. C. Three-Dimensional Structure of Recombinant Human Muscle Fatty Acid-binding Protein. J. Biol. Chem. 1992, 267, 18541-18550.
13. Young, A. C. M.; Scapin, G.; Kromminga, A.; Patel, S. B.; Veerkamp, J. H.; Sacchettini, J. C. Structural Studies on Human Muscle Fatty Acid Binding Protein at 1.4 A˚ Resolution: Binding Interactions with Three C18 Fatty Acids. Structure 1994, 2, 523-534.
14. Scapin, G.; Young, A. C. M.; Kromminga, A.; Veerkamp, J. H.; Gordon, J. I.; Sacchettini, J. C. High Resolution X-ray Studies of Mammalian Intestinal and Muscle Fatty Acid-Binding Proteins Provide an Opportunity for Defining the Chemical Nature of Fatty Acid: Protein Interactions. Mol. Cell. Biochem. 1993, 123, 3-13.
15. Hirose, M.; Sugiyama, S.; Ishida, H.; Niiyama, M.; Matsuoka, D.; Hara, T.; Mizohata, E.; Murakami, S.; Inoue, T.; Matsuoka, S.; Murata, M. Structure of the Human-Heart Fatty-Acid-Binding Protein 3 in Complex with the Fluorescent Probe 1-Anilinonaphthalene-8-Sulphonic Acid. J. Synchrotron Radiat. 2013, 20, 923-928.
16. Lassen, D.; Lücke, C.; Kveder, M.; Mesgarzadeh, A.; Schmidt, J. M.; Specht, B.; Lezius, A.; Spener, F.; Rüterjans, H. Three-Dimensional Structure of Bovine Heart Fatty-Acid-Binding Protein with Bound Palmitic Acid, Determined by Multidimensional NMR Spectroscopy. Eur. J. Biochem. 1995, 230, 266-280.
17. Woolf, T. B. Simulations of Fatty Acid-Binding Proteins Suggest Sites Important for Function. I. Stearic Acid. Biophys. J. 1998, 74, 681-693.
18. Schaap, F. G.; van der Vusse, G. J.; Glatz, J. F. C. Evolution of the Family of Intracellular Lipid Binding Proteins in Vertebrates. Mol. Cell. Biochem. 2002, 239, 69-77.
19. Balendiran, G. K.; Schnütgen, F.; Scapin, G.; Börchers, T.; Xhong, N.; Lim, K.; Godbout, R.; Spener, F.; Sacchettini, J. C. Crystal Structure and Thermodynamic Analysis of Human Brain Fatty Acid-Binding Protein. J. Biol. Chem. 2000, 275, 27045-27054.
20. Marr, E.; Tardie, M.; Carty, M.; Philips, T. B.; Wang, I.-K.; Soeller, W.; Qiu, X.; Karam, G. Expression, Purification, Crystallization and Structure of Human Adipocyte Lipid-Binding Protein (aP2). Acta Crystallogr. F 2006, 62, 1058-1060.
21. Hohoff, C.; Börchers, T.; Rüstow, B.; Spener, F.; van Tilbeurgh, H. Expression, Purification, and Crystal Structure Determination of Recombinant Human Epidermal-Type Fatty Acid Binding Protein. Biochemistry 1999, 38, 12229-12239.
22. Ruskamo, S.; Yadav, R. P.; Sharma, S.; Lehtimäki, M.; Laulumaa, S.; Aggarwal, S.; Simons, M.; Bürck, J.; Ulrich, A. S.; Juffer, A. H.; Kursula, I.; Kursula, P. Atomic Resolution View Into the Structure-Function Relationships of the Human Myelin Peripheral Membrane Protein P2. Acta Crystallogr. D 2014, 70, 165-176.
23. Lücke, C.; Huang, S.; Rademacher, M.; Rüterjans, H. New Insights into Intracellular Lipid Binding Proteins: The Role of Buried Water. Protein Sci. 2002, 11, 2383-2392.
24. Chaplin, M. Do We Underestimate the Importance of Water in Cell Biology? Nat. Rev. Mol. Cell Biol. 2006, 7, 861-866.
25. Ball, P. Water as an Active Constituent in Cell Biology. Chem. Rev. 2008, 108, 74-108.
26. Williams, M. A.; Goodfellow, J. M.; Thornton, J. M. Buried Waters and Internal Cavities in Monomeric Proteins. Protein Sci. 1994, 3, 1224-1235.
27. Bhat, T. N.; Bentley, G. A.; Boulot, G.; Greene, M. I.; Tello, D.; Dall'Acqua, W.; Souchon, H.; Schwarz, F. P.; Mariuzza, R. A.; Poljak, R. J. Bound Water Molecules and Conformational Stabilization Help Mediate an Antigen-Antibody Association. Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 1089-1093.
28. Takano, K.; Yamagata, Y.; Funahashi, J.; Hioki, Y.; Kuramitsu, S.; Yutani, K. Contribution of Intra- and Intermolecular Hydrogen Bonds to the Conformational Stability of Human Lysozyme. Biochemistry 1999, 38, 12698-12708.
29. Ricchiuto, P.; Rocco, A. G.; Gianazza, E.; Corrada, D.; Beringhelli, T.; Eberini, I. Structural and Dynamic Roles of Permanent Water Molecules in Ligand Molecular Recognition by Chicken Liver Bile Acid Binding Protein. J. Mol. Recognit. 2008, 21, 348-354.
30. Gillilan, R. E.; Ayers, S. D.; Noy, N. Structural Basis for Activation of Fatty Acid-Binding Protein 4. J. Mol. Biol. 2007, 372, 1246-1260.
31. Ory, J. J.; Banaszak, L. J. Studies of the Ligand Binding Reaction of Adipocyte Lipid Binding Protein Using the Fluorescent Probe 1,8-Anilinonaphthalene-8-Sulfonate. Biophys. J. 1999, 77, 1107-1116.
32. Lehmann, F.; Haile, S.; Axen, E.; Medina, C.; Uppenberg, J.; Svensson, S.; Lundbäck, T.; Rondahl, L.; Barf, T. Discovery of Inhibitors of Human Adipocyte Fatty Acid-Binding Protein, a Potential Type 2 Diabetes Target. Bioorg. Med. Chem. Lett. 2004, 14, 4445-4448.
33. Barf, T.; Lehmann, F.; Hammer, K.; Haile, S.; Axen, E.; Medina, C.; Uppenberg, J.; Svensson, S.; Rondahl, L.; Lundbäck, T. N-Benzyl-Indolo Carboxylic Acids: Design and Synthesis of Potent and Selective Adipocyte Fatty-Acid Binding Protein (A-FABP) Inhibitors. Bioorg. Med. Chem. Lett. 2009, 19, 1745-1748.
34. Xu, Z.; Bernlohr, D. A.; Banaszak, L. J. The Adipocyte Lipid-Binding Protein at 1.6-A˚ Resolution. Crystal Structures of the Apoprotein and with Bound Saturated and Unsaturated Fatty Acids. J. Biol. Chem. 1993, 268, 7874-7884.
35. Armstrong, E. H.; Goswami, D.; Griffin, P. R.; Noy, N.; Ortlund, E. A. Structural Basis for Ligand Regulation of the Fatty Acid-binding Protein 5, Peroxisome Proliferator-Activated Receptor β/δ (FABP5-PPARβ/δ) Signaling Pathway. J. Biol. Chem. 2014, 289, 14941-14954.
36. Ragona, L.; Pagano, K.; Tomaselli, S.; Favretto, F.; Ceccon, A.; Zanzoni, S.; D'Onofrio, M.; Assfalg, M.; Molinari, H. The Role of Dynamics in Modulating Ligand Exchange in Intracellular Lipid Binding Proteins. Biochim. Biophys. Acta 2014, 1844, 1268-1278.
37. Sacchettini, J. C.; Scapin, G.; Gopaul, D.; Gordon, J. I. Refinement of the Structure of Escherichia coli-Derived Rat Intestinal Fatty Acid Binding Protein with Bound Oleate to 1.75-A˚ Resolution. Correlation with the Structures of the Apoprotein and the Protein with Bound Palmitate. J. Biol. Chem. 1992, 267, 23534-23545.
38. Constantine, K. L.; Friedrichs, M. S.; Wittekind, M.; Jamil, H.; Chu, C.-H.; Parker, R. A.; Goldfarb, V.; Mueller, L.; Farmer, B. T., II Backbone and Side Chain Dynamics of Uncomplexed Human Adipocyte and Muscle Fatty Acid-Binding Proteins. Biochemistry 1998, 37, 7965-7980.
39. Reese-Wagoner, A.; Thompson, J.; Banaszak, L. Structural Properties of the Adipocyte Lipid Binding Protein. Biochim. Biophys. Acta 1999, 1441, 106-116.
40. Jenkins, A. E.; Hockenberry, J. A.; Nguyen, T.; Bernlohr, D. A. Testing of the Portal Hypothesis: Analysis of a V32G, F57G, K58G Mutant of the Fatty Acid Binding Protein of the Murine Adipocyte. Biochemistry 2002, 41, 2022-2027.
41. Friedman, R.; Nachliel, E.; Gutman, M. Molecular Dynamics Simulations of the Adipocyte Lipid Binding Protein Reveal a Novel Entry Site for the Ligand. Biochemistry 2005, 44, 4275-4283.
42. Fiedman, R.; Nachliel, E.; Gutman, M. Fatty Acid Binding Proteins: Same Structure but Different Binding Mechanisms? Molecular Dynamics Simulations of Intestinal Fatty Acid Binding Protein. Biophys. J. 2006, 90, 1535-1545.
43. Tsfadia, Y.; Friedman, R.; Kadmon, J.; Selzer, A.; Nachiel, E.; Gutman, M. Molecular Dynamics Simulations of Palmitate Entry into the Hydrophobic Pocket of the Fatty Acid Binding Protein. FEBS Lett. 2007, 581, 1243-1247.
44. Di Pietro, S. M.; Córsico, B.; Perduca, M.; Monaco, H. L.; Santomé, J. A. Structural and Biochemical Characterization of Toad Liver Basic Fatty Acid-Binding Protein. Biochemistry 2003, 42, 8192-8203.
45. Lücke, C.; Fushman, D.; Ludwig, C.; Hamilton, J. A.; Sacchettini, J. C.; Rütherjans, H. A Comparative Study of the Backbone Dynamics of Two Closely Related Lipid Binding Proteins: Bovine Heart Fatty Acid Binding Protein and Porcine Ileal Lipid Binding Protein. Mol. Cell. Biochem. 1999, 192, 109-121.
46. Zamarreño, F.; Herrera, F. E.; Córsico, B.; Costabel, M. D. Similar Structures but Different Mechanisms. Prediction of FABPs-Membrane Interaction by Electrostatic Calculation. Biochim. Biophys. Acta 2012, 1818, 1691-1697.
47. Ferrolino, M. C.; Zhuravleva, A.; Budyak, I. L.; Krishnan, B.; Gierasch, L. M. Delicate Balance between Functionally Required Flexibility and Aggregation Risk in a β-Rich Protein. Biochemistry 2013, 52, 8843-8854.
48. Woolf, T. B.; Grossfield, A.; Tychko, M. Differences Between Apo and Three Holo Forms of the Intestinal Fatty Acid Binding Protein Seen by Molecular Dynamics Computer Calculations. Biophys. J. 2000, 78, 608-625.
49. Bakowies, D.; van Gunsteren, W. F. Simulations of Apo and Holo-Fatty Acid Binding Protein: Structure and Dynamics of Protein, Ligand and Internal Water. J. Mol. Biol. 2002, 315, 713-736.
50. a values. J. Chem. Theory Comput. 2011, 7, 2284-2295.
51. Ikeguchi, M. Partial Rigid-Body Dynamics in NPT, NPAT and NPγT Ensembles for Protein and Membranes. J. Comput. Chem. 2004, 25, 259-529.
52. 2 Dihedral Angles. J. Chem. Theory Comput. 2012, 8, 3257-3273.
53. Klauda, J. B.; Venable, R. M.; Freites, J. A.; O'Connor, J. W.; Tobias, D. J.; Mondragon-Ramirez, C.; Vorobyov, I.; MacKerell, A. D., Jr.; Pastor, R. W. Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types. J. Phys. Chem. B 2010, 114, 7830-7843.
54. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water. J. Chem. Phys. 1983, 79, 926-935.
55. Marthyna, G. J.; Tobias, D. J.; Klein, M. L. Constant Pressure Molecular Dynamics Algorithms. J. Chem. Phys. 1994, 101, 4177-4189.
56. Lee, B.; Richards, F. M. The Interpretation of Protein Structures: Estimation of Static Accessibility. J. Mol. Biol. 1971, 55, 379-400.
57. Kabsch, W. A Solution for the Best Rotation to Relate Two Sets of Vectors. Acta Crystallogr. A 1976, 32, 922-923.
58. Kabsch, W. A Discussion of the Solution for the Best Rotation to Relate Two Sets of Vectors. Acta Crystallogr. A 1978, 34, 827-828.
59. Matsuoka, D.; Nakasako, M. Prediction of Hydration Structures around Hydrophilic Surfaces of Proteins by Using the Empirical Hydration Distribution Functions from a Database Analysis. J. Phys. Chem. B 2010, 114, 4652-4663.
60. Finney, J. L. Water? What's So Special about It? Philos. Trans. R. Soc. London B 2004, 359, 1145-1165.
61. Matsuoka, D.; Nakasako, M. Probability Distributions of Hydration Water Molecules around Polar Protein Atoms Obtained by a Database Analysis. J. Phys. Chem. B 2009, 113, 11274-11292.
62. Bakowies, D.; van Gunsteren, W. F. Water in Protein Cavities: A Procedure to Identify Internal Water and Exchange Pathways and Application to Fatty Acid-Binding Protein. Proteins: Struct., Funct., Bioinf. 2002, 47, 534-545.
63. Lounnas, V.; Pettitt, B. M. A Connected-Cluster of Hydration around Myoglobin: Correlation between Molecular Dynamics Simulations and Experiment. Proteins: Struct., Funct., Genet. 1994, 18, 133-147.
64. Higo, J.; Nakasako, M. Hydration Structure of Human Lysozyme Investigated by Molecular Dynamics Simulation and Cryogenic X-ray Crystal Structure Analyses: on the Correlation between and Crystal Water Sites, Solvent Density and Solvent Dipole. J. Comput. Chem. 2002, 23, 1323-1336.
65. Yokomizo, T.; Nakasako, M.; Yamazaki, T.; Shindo, H.; Higo, J. Hydrogen-Bond Patterns in the Hydration Structure of a Protein. Chem. Phys. Lett. 2005, 401, 332-336.
66. Yokomizo, T.; Higo, J.; Nakasako, M. Patterns and Networks of Hydrogen-Bonds in the Hydration Structure of Human Lysozyme. Chem. Phys. Lett. 2005, 410, 31-35.
67. Hodsdon, M. E.; Cistola, D. P. Discrete Backbone Disorder in the Nuclear Magnetic Resonance Structure of Apo Intestinal Fatty Acid-Binding Protein: Implications for the Mechanism of Ligand Entry. Biochemistry 1997, 36, 1450-1460.
68. Lu, J.; Lin, C.-L.; Tang, C.; Ponder, J. W.; Kao, J. L. F.; Cistola, D. P.; Li, E. Binding of Retinol Induces Changes in Rat Cellular Retinol-binding Protein II Conformation and Backbone Dynamics. J. Mol. Biol. 2000, 300, 619-632.
69. Franzoni, L.; Lücke, C.; Pérez, C.; Cavazzini, D.; Rademacher, M.; Ludwig, C.; Spisni, A.; Rossi, G. L.; Rüterjans, H. Structure and Backbone Dynamics of Apo- and Holo-cellular Retinol-binding Protein in Solution. J. Biol. Chem. 2002, 277, 21983-21997.
70. Otting, G.; Liepinsh, E.; Wüthrich, K. Protein Hydration in Aqueous Solution. Science 1991, 254, 974-980.
71. Denisov, V. P.; Halle, B. Protein Hydration Dynamics in Aqueous Solution. Faraday Discuss. 1996, 103, 227-244.
72. Halle, B. Protein Hydration Dynamics in Solution: a Critical Survey. Philos. Trans. R. Soc. London B 2004, 359, 1207-1224.
73. Sinha, S. K.; Bandyopadhyay, S. Dynamic Properties of Water around a Protein-DNA Complex from Molecular Dynamics Simulations. J. Chem. Phys. 2011, 135, 135101.
74. Kohn, J. E.; Afonine, P. V.; Ruscio, J. Z.; Adams, P. D.; Head-Gordon, T. Evidence of Functional Protein Dynamics from X-ray Crystallographic Ensembles. PLoS Comput. Biol. 2010, 6, e1000911.
75. Garman, E. 'Cool' Crystals: Macromolecular Cryocrystallography and Radiation Damage. Curr. Opin. Struct. Biol. 2003, 13, 545-551.
76. Halle, B. Biomolecular Cryocrystallography: Structural Changes during Flash-Cooling. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 4793-4798.
77. Friedmanm, R.; Caflisch, A. On the Orientation of the Catalytic Dyad in Aspartic Proteases. Proteins 2010, 78, 1575-1582.
78. D'Onofrio, M.; Ragona, L.; Fessas, D.; Signorelli, M.; Ugolini, R.; Pedò, M.; Assfalg, M.; Molinari, H. NMR Unfolding Studies on a Liver Bile Acid Binding Protein Reveal a Global Two-State Unfolding and Localized Singular Behaviors. Arch. Biochem. Biophys. 2009, 481, 21-29.
79. Zimmerman, A. W.; Rademacher, M.; Rüterjans, H.; Lücke, C.; Veerkamp, J. H. Functional and Conformational Characterization of New Mutants of Heart Fatty Acid-Binding Protein. Biochem. J. 1999, 344, 495-501.
80. Franchini, G. R.; Storch, J.; Corsico, B. The Integrity of the α-Helical Domain of Intestinal Fatty Acid Binding Pocket Is Essential for the Collision-Mediated Transfer of Fatty Acids to Phospholipid Membranes. Biochim. Biophys. Acta 2008, 1781, 192-199.
81. Liou, H.-L.; Kahn, P. C.; Storch, J. Role of the Helical Domain in Fatty Acid Transfer from Adipocyte and Heart Fatty Acid-binding Proteins to Membrane. J. Biol. Chem. 2002, 277, 1806-1815.
82. Tan, N.-S.; Shaw, N. S.; Vinckenbosch, N.; Liu, P.; Yasmin, R.; Desvergne, B.; Wahli, W.; Noy, N. Selective Cooperation between Fatty Acid Binding Proteins and Peroxisome Proliferator-Activated Receptors in Regulating Transcription. Mol. Cell. Biol. 2002, 22, 5114-5127.