Molecular simulations of β-lactoglobulin complexed with fatty acids reveal the structural basis of ligand affinity to internal and possible external binding sites

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 10, 2014, Pages 2609-2619

  Evoli, Stefania ^a   Guzzi, Rita ^a   Rizzuti, Bruno ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

Author keywords

Binding sites; Fatty acids; Molecular docking; Molecular dynamics simulation; lactoglobulin

Indexed keywords

BETA LACTOGLOBULIN; DECANOIC ACID; HYDROCARBON; LAURIC ACID; LYSINE; MYRISTIC ACID; OCTANOIC ACID; PALMITIC ACID; SATURATED FATTY ACID; STEARIC ACID; FATTY ACID; LACTOGLOBULIN; LIGAND; METHIONINE; PHENYLALANINE; STEARIC ACID DERIVATIVE;

ALPHA HELIX; ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTALLIZATION; HYDROPHOBICITY; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE; STATIC ELECTRICITY; ANIMAL; BOVINE; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; METABOLISM; MOLECULAR WEIGHT; SURFACE PROPERTY;

ANIMALS; BINDING SITES; CATTLE; FATTY ACIDS, NONESTERIFIED; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; LACTOGLOBULINS; LIGANDS; LYSINE; METHIONINE; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR WEIGHT; PALMITIC ACID; PHENYLALANINE; PROTEIN CONFORMATION; STATIC ELECTRICITY; STEARIC ACIDS; SURFACE PROPERTIES;

EID: 84934942834     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24625     Document Type: Article

References (53)

1. Flower DR. The lipocalin protein family: structure and function. Biochem J 1996;318:1-14.
2. Pérez MD, Calvo M. Interaction of β-lactoglobulin with retinol and fatty acids and its role as a possible biological function for this protein: a review. J Dairy Sci 1995;78:978-988.
3. Rocha TL, Paterson G, Crimmins K, Boyd A, Sawyer L, Fothergill-Gilmore LA. Expression and secretion of recombinant ovine β-lactoglobulin in Saccharomyces cerevisiae and Kluyveromyces lactis. Biochem J 1996;313:927-932.
4. Brownlow S, Cabral JHM, Cooper R, Flower DR, Yewdall SJ, Polikarpov I, North AC, Sawyer L. Bovine β-lactoglobulin at 1.8 Å resolution-still an enigmatic lipocalin. Structure 1997;5:481-495.
5. Kontopidis G, Holt C, Sawyer L. Invited review: β-lactoglobulin: binding properties, structure, and function. J Dairy Sci 2004;87:785-796.
6. Qin BY, Bewley MC, Creamer LK, Baker HM, Baker EN, Jameson GB. Structural basis of the Tanford transition of bovine β-lactoglobulin. Biochemistry 1998;37:14014-14023.
7. Wu SY, Pérez MD, Puyol P, Sawyer L. β-lactoglobulin binds palmitate within its central cavity. J Biol Chem 1999;274:170-174.
8. Kontopidis G, Holt C, Sawyer L. The ligand-binding site of bovine β-lactoglobulin: evidence for a function? J Mol Biol 2002;318:1043-1055.
9. Loch JI, Polit A, Bonarek P, Olszewska D, Kurpiewska K, Dziedzicka-Wasylewska M, Lewiński K. Structural and thermodynamic studies of binding saturated fatty acids to bovine β-lactoglobulin. Int J Biol Macromol 2012;50:1095-1102.
10. Frapin D, Dufour E, Haertle T. Probing the fatty acid binding site of β-lactoglobulins. J Protein Chem 1993;12:443-449.
11. Narayan M, Berliner LJ. Mapping fatty acid binding to β-lactoglobulin: ligand binding is restricted by modification of Cys 121. Protein Sci 1998;7:150-157.
12. Qin BY, Creamer LK, Baker EN, Jameson GB. 12-Bromododecanoic acid binds inside the calyx of bovine β-lactoglobulin. FEBS Lett 1998;438:272-278.
13. Wang QWQ, Allen JC, Swaisgood HE. Protein concentration dependence of palmitate binding to β-lactoglobulin. J Dairy Sci 1998;81:76-81.
14. 3 binding site of milk β-lactoglobulin. Proteins 2008;71:1197-1210.
15. 3 complex: revealing a secondary binding site. Cryst Growth Des 2008;8:4268-4276.
16. Dufour E, Roger P, Haertlé T. Binding of benzo(α)pyrene, ellipticine, and cis-parinaric acid to β-lactoglobulin: influence of protein modifications. J Protein Chem 1992;11:645-652.
17. Mandalari G, Mackie AM, Rigby NM, Wickham MSJ, Mills ENC. Physiological phosphatidylcholine protects bovine β-lactoglobulin from simulated gastrointestinal proteolysis. Mol Nutr Food Res 2009;53:131-139.
18. Loch J, Polit A, Górecki A, Bonarek P, Kurpiewska K, Dziedzicka-Wasylewska M, Lewiński K. Two modes of fatty acid binding to bovine β-lactoglobulin-crystallographic and spectroscopic studies. J Mol Recognit 2011;24:341-349.
19. a calculations. Proteins 2004;54:744-758.
20. Bello M, Portillo-Téllez MD, García-Hernández E. Energetics of ligand recognition and self-association of bovine β-lactoglobulin: differences between variants A and B. Biochemistry 2011;50:151-161.
21. Bello M, Gutiérrez G, García-Hernández E. Structure and dynamics of β-lactoglobulin in complex with dodecyl sulfate and laurate: a molecular dynamics study. Biophys Chem 2012;165:79-86.
22. Sahihi M, Heidari-Koholi Z, Bordbar AK. The interaction of polyphenol flavonoids with β-lactoglobulin: molecular docking and molecular dynamics simulation studies. J Macromol Sci B 2012;51:2311-2323.
23. Guzzi R, Rizzuti B, Bartucci R. Dynamics and binding affinity of spin-labeled stearic acids in β-lactoglobulin: evidences from EPR spectroscopy and molecular dynamics simulation. J Phys Chem B 2012;116:11608-11615.
24. Bello M, García-Hernández E. Ligand entry into the calyx of β-lactoglobulin. Biopolymers 2014;101:744-757.
25. Bello M. Binding free energy calculations between bovine β-lactoglobulin and four fatty acids using the MMGBSA method. Biopolymers, Accepted Article, DOI: 10.1002/bip.22483.
26. Hu WB, Liu JA, Luo Q, Han YM, Wu K, Lv S, Xiong SX, Wang FY. Elucidation of the binding sites of sodium dodecyl sulfate to β-lactoglobulin using hydrogen/deuterium exchange mass spectrometry combined with docking simulation. Rapid Commun Mass Sp 2011;25:1429-1436.
27. Domínguez-Ramírez L, Del Moral-Ramírez E, Cortes-Hernández P, García-Garibay M, Jiménez-Guzmán J. β-lactoglobulin's conformational requirements for ligand binding at the calyx and the dimer interphase: a flexible docking study. PLoS One 2013;8:e79530.
28. Barbiroli A, Bonomi F, Ferranti P, Fessas D, Nasi A, Rasmussen P, Iametti S. Bound fatty acids modulate the sensitivity of bovine β-lactoglobulin to chemical and physical denaturation. J Agr Food Chem 2011;59:5729-5737.
29. Collini M, D'Alfonso L, Molinari H, Ragona L, Catalano M, Baldini G. Competitive binding of fatty acids and the fluorescent probe 1-8-anilinonaphthalene sulfonate to bovine β-lactoglobulin. Protein Sci 2003;12:1596-1603.
30. Trott O, Olson AJ. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 2010;31:455-461.
31. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 1998;19:1639-1662.
32. Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, Shirts MR, Smith JC, Kasson PM, van der Spoel D, Hess B, Lindahl E. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 2013;29:845-854.
33. Oostenbrink C, Villa A, Mark AE, Van Gunsteren WF. A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. J Comput Chem 2004;25:1656-1676.
34. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph Model 1996;14:33-38.
35. DeLano WL. The PyMOL molecular graphics system. DeLano Scientific, Palo Alto, CA; 2002.
36. Rizzuti B, Pantusa M, Guzzi R. The role of Lys525 on the head-group anchoring of fatty acids in the highest affinity binding site of albumin. Spectrosc-Int J 2010;24:159-163.
37. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J. Interaction models for water in relation to protein hydration. In: Pullman B, editor. Intermolecular forces. Dordrecht: Reidel; 1981. pp 331-342.
38. Bussi G, Donadio D, Parrinello M. Canonical sampling through velocity rescaling. J Chem Phys 2007;126:0140101.
39. Berendsen HJC, Postma JPM, van Gunsteren WF, Di Nola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984;81:3684-3690.
40. Darden T, York D, Pedersen L. Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems. J Chem Phys 1993;98:10089-10092.
41. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A smooth particle mesh Ewald method. J Chem Phys 1995;103:8577-8593.
42. Hess B. P-LINCS: A parallel linear constraint solver for molecular simulation. J Chem Theory Comput 2008;4:116-122.
43. García AE. Large-amplitude nonlinear motions in proteins. Phys Rev Lett 1992;68:2696-2699.
44. Amadei A, Linssen ABM, Berendsen HJC. Essential dynamics of proteins. Proteins 1993;17:412-425.
45. Jameson GB, Adams JJ, Creamer LK. Flexibility, functionality and hydrophobicity of bovine β-lactoglobulin. Int Dairy J 2002;12:319-329.
46. Qvist J, Davidovic M, Hamelberg D, Halle B. A dry ligand-binding cavity in a solvated protein. Proc Natl Acad Sci USA 2008;105:6296-6301.
47. Konuma T, Sakurai K, Goto Y. Promiscuous binding of ligands by β-lactoglobulin involves hydrophobic interactions and plasticity. J Mol Biol 2007;368:209-218.
48. Rashin AA, Rashin AHL, Jernigan RL. Protein flexibility: coordinate uncertainties and interpretation of structural differences. Acta Crystallogr D 2009;65:1140-1161.
49. Ragona L, Fogolari F, Zetta L, Pérez DM, Puyol P, De Kruif K, Löhr F, Rüterjans H, Molinari H. Bovine β-lactoglobulin: interaction studies with palmitic acid. Protein Sci 2000;9:1347-1356.
50. Sakurai K, Konuma T, Yagi M, Goto Y. Structural dynamics and folding of β-lactoglobulin probed by heteronuclear NMR. Biochim Biophys Acta-Gen Subj 2009;1790:527-537.
51. Edwards PB, Creamer LK, Jameson GB. Structure and stability of whey proteins. In: Thompson A, Boland M, Singh H, editors. Milk proteins-from expression to food. Academic Press: San Diego; 2009. pp 163-203.
52. Yang MC, Chen NC, Chen CJ, Wu CY, Mao SJT. Evidence for β-lactoglobulin involvement in vitamin D transport in vivo-role of the γ-turn (Leu-Pro-Met) of β-lactoglobulin in vitamin D binding. FEBS J 2009;276:2251-2265.
53. Wu XL, Dey R, Wu H, Liu ZG, He QQ, Zeng XJ. Studies on the interaction of -epigallocatechin-3-gallate from green tea with bovine β-lactoglobulin by spectroscopic methods and docking. Int J Dairy Technol 2013;66:7-13.