Structural and energetic requirements for a second binding site at the dimeric β-lactoglobulin interface

Journal of Biomolecular Structure and Dynamics

Volumn 34, Issue 9, 2016, Pages 1884-1902

  Bello, Martiniano ^a  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

binding free energy; blind docking; lactoglobulin; molecular dynamics simulations; VD3

Indexed keywords

BETA LACTOGLOBULIN; COLECALCIFEROL; LACTOGLOBULIN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; DECOMPOSITION; DIMERIZATION; ENERGY; HYDROGEN BOND; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; OXIDATIVE COUPLING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STOICHIOMETRY; STRUCTURE ANALYSIS; CHEMICAL PHENOMENA; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; STRUCTURE ACTIVITY RELATION;

BINDING SITES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LACTOGLOBULINS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84953227198     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2015.1094413     Document Type: Article

References (63)

1. C.Barbana, M.D.Pérez, L.Sánchez, M.Dalgalarrondo, J.M.Chobert, T.Haertlé, … M.Calvo, (2006). Interaction of bovine [alpha]-lactalbumin with fatty acids as determined by partition equilibrium and fluorescence spectroscopy. International Dairy Journal, 16, 18–25. doi:10.1016/j.idairyj.2005.01.007
2. A.Barbiroli, T.Beringhelli, F.Bonomi, D.Donghi, P.Ferranti, M.Galliano, … M.C.Vilardo, (2000). Bovine beta-lactoglobulin acts as an acid-resistant drug carrier by exploiting its diverse binding regions. Biological Chemistry, 391, 21–32. doi:10.1515/BC.2010.008
3. M.Bello, (2014). Binding free energy calculations between bovine β-lactoglobulin and four fatty acids using the MMGBSA method. Biopolymers, 101, 1010–1018. doi:10.1002/bip.22483
4. M.Bello, J.Correa-Basurto, & E.Rudiño-Piñera, (2014). Simulation of the cavity-binding site of three bacterial upon complex stabilization:Interactional profile and electron transference pathways. Journal of Biomolecular Structure & Dynamics, 32, 1303–1317. doi:10.1080/07391102.2013.817954
5. M.Bello, & E.García-Hernández, (2014). Ligand entry into the calyx of β-lactoglobulin. Biopolymers, 101, 744–757. doi:10.1002/bip.22454
6. M.Bello, G.Gutiérrez, & E.García-Hernández, (2012). Structure and dynamics of β-lactoglobulin in complex with dodecyl sulfate and laurate:A molecular dynamics study. Biophysical Chemistry, 165–166, 79–86. doi:10.1016/j.bpc.2012.03.009
7. M.Bello, G.Pérez-Hernández, D.A.Fernández-Velasco, R.Arreguín-Espinosa, & E.García-Hernández, (2008). Energetics of protein homodimerization:Effects of water sequestering on the formation of beta-lactoglobulin dimer. Proteins, 70, 1475–1487. doi:10.1002/prot.21639
8. M.Bello, M.Martínez-Archundia, & J.Correa-Basurto, (2013). Automated docking for novel drug discovery. Expert Opinion on Drug Discovery, 8, 821–834. doi:10.1517/17460441.2013.794780
9. M.Bello, M.D.Portillo-Téllez, & E.García-Hernández, (2011). Energetics of ligand recognition and self-association of bovine β-lactoglobulin:Differences between variants A and B. Biochemistry, 50, 151–161. doi:10.1021/bi1016155
10. H.J.C.Berendsen, J.P.M.Postma, W.F.van Gunsteren, A.DiNola, & J.R.Haak, (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81, 3684–3690. doi:10.1063/1.448118
11. S.Brownlow, J.H.M.Cabral, R.Cooper, D.R.Flower, S.J.Yewdall, I.Polikarpov, … L.Sawyer, (1997). Bovine β-lactoglobulin at 1.8 Å resolution – Still an enigmatic lipocalin. Structure, 5, 481–495. doi:10.1016/S0969-2126(97)00205-0
12. D.A.Case, T.E.Cheatham, T.Darden, H.Gohlke, R.Luo, K.M.Merz, Jr., … R.J.Woods, (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26, 1668–1688. doi:10.1002/jcc.20290
13. M.Collini, L.D’Alfonso, H.Molinari, L.Ragona, M.Catalano, & G.Baldini, (2003). Competitive binding of fatty acids and the fluorescent probe 1-8-anilinonaphthalene sulfonate to bovine β-lactoglobulin. Protein Science, 12, 1596–1603. doi:10.1110/ps.0304403
14. T.Darden, D.York, & L.Pedersen, (1993). Particle mesh Ewald:An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98, 10089–10092. doi:10.1063/1.464397
15. W.L.DeLano, (2002). The PyMOL molecular graphics system. Palo Alto, CA:DeLano Scientific.
16. L.Domínguez-Ramírez, E.Del Moral-Ramírez, P.Cortes-Hernández, M.García-Garibay, & J.Jiménez-Guzmán, (2013). β-lactoglobulin’s conformational requirements for ligand binding at the calyx and the dimer interphase:A flexible docking study. PLoS ONE, 8, e79530. doi:10.1371/journal.pone.0079530
17. Y.Duan, C.Wu, S.Chowdhury, M.C.Lee, G.Xiong, W.Zhang, … P.Kollman, (2003). A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. Journal of Computational Chemistry, 24, 1999–2012. doi:10.1002/jcc.10349
18. C.Eigenbrot, M.Randal, & A.A.Kossiakoff, (1992). Structural effects induced by mutagenesis affected by crystal packing factors:The structure of a 30-51 disulfide mutant of basic pancreatic trypsin inhibitor. Proteins, 14, 75–87. doi:10.1002/prot.340140109
19. S.Evoli, R.Guzzi, & B.Rizzuti, (2014). Molecular simulations of β-lactoglobulin complexed with fatty acids reveal the structural basis of ligand affinity to internal and possible external binding sites. Proteins, 82, 2609–2619. doi:10.1002/prot.24625
20. H.R.Faber, & B.W.Matthews, (1990). A mutant T4 lysozyme displays five different crystal conformations. Nature, 348, 263–266. doi:10.1038/348263a0
21. J.S.Fraser, H.van den Bedem, A.J.Samelson, P.T.Lang, J.M.Holton, N.Echols, … T.Alber, (2011). Accessing protein conformational ensembles using room-temperature X-ray crystallography. Proceedings of the National Academy of Sciences, 108, 16247–16252. doi:10.1073/pnas.1111325108
22. H.Gohlke, & D.A.Case, (2004). Converging free energy estimates:MM-PB(GB)SA studies on the protein–protein complex Ras-Raf. Journal of Computational Chemistry, 25, 238–250. doi:10.1002/jcc.10379
23. A.W.Götz, M.J.Williamson, D.Xu, D.Poole, S.Le Grand, & R.C.Walker, (2012). Routine microsecond molecular dynamics simulations with AMBER-Part I:Generalized born. Journal of Chemical Theory and Computation, 8, 1542–1555. doi:10.1021/ct200909j
24. G.Gutiérrez-Magdaleno, M.Bello, M.C.Portillo-Téllez, A.Rodríguez-Romero, & E.García-Hernández, (2013). Ligand binding and self-association cooperativity of β-lactoglobulin. Journal of Molecular Recognition, 26, 67–75. doi:10.1002/jmr.2249
25. G.B.Jameson, J.J.Adams, & L.K.Creamer, (2002). Flexibility, functionality and hydrophobicity of bovine β-lactoglobulin. International Dairy Journal, 12, 319–329. doi:10.1016/S0958-6946(02)00028-6
26. W.L.Jorgensen, J.Chandrasekhar, J.D.Madura, R.W.Impey, & M.L.Klein, (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79, 926–935. doi:10.1063/1.445869
27. J.K.Keppler, T.Koudelka, K.Palani, M.C.Stuhldreier, F.Temps, A.Tholey, … K.Schwarz, (2014). Characterization of the covalent binding of allyl isothiocyanate to β-lactoglobulin by fluorescence quenching, equilibrium measurement, and mass spectrometry. Journal of Biomolecular Structure and Dynamics, 32, 1103–1117. doi:10.1080/07391102.2013.809605
28. S.Khorsand Ahmadi, M.Mahmoodian Moghadam, P.Mokaberi, M.Reza Saberi, & J.Chamani, (2015). A comparison study of the interaction between β-lactoglobulinand retinol at two different conditions:Spectroscopic and molecular modeling approaches. Journal of Biomolecular Structure and Dynamics, 33, 1880–1898. doi:10.1080/07391102.2014.977351
29. P.A.Kollman, I.Massova, C.Reyes, B.Kuhn, S.Huo, L.Chong, … T.E.Cheatham, 3rd. (2000). Calculating structures and free energies of complex molecules:Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33, 889–897. doi:10.1021/ar000033j
30. G.Kontopidis, C.Holt, & L.Sawyer, (2002). The ligand-binding site of bovine β-lactoglobulin:Evidence for a function? Journal of Molecular Biology, 318, 1043–1055. doi:10.1016/S0022-2836(02)00017-7
31. G.Kontopidis, C.Holt, & L.Sawyer, (2004). β-Lactoglobulin:Binding properties, structure, and function. Journal of Dairy Science, 87, 785–796. doi:10.3168/jds.S0022-0302(04)73222-1
32. K.Kuwata, M.Hoshino, S.Era, C.A.Batt, & Y.Goto, (1998). α→β Transition of β-lactoglobulin as evidenced by heteronuclear NMR. Journal of Molecular Biology, 283, 731-739. doi:10.1006/jmbi.1998.211710.1006/jmbi.1998.2117
33. K.Kuwata, M.Hoshino, V.Forge, S.Era, C.A.Batt, & Y.Goto, (1999). Solution structure and dynamics of bovine β-lactoglobulin A. Protein Science, 8, 2541–2545. doi:10.1110/ps.8.11.2541
34. J.Li, J.J.Correia, L.Wang, J.O.Trent, & J.B.Chaires, (2005). Not so crystal clear:The structure of the human telomere G-quadruplex in solution differs from that present in a crystal. Nucleic Acids Research, 33, 4649–4659. doi:10.1093/nar/gki782
35. J.I.Loch, A.Polit, P.Bonarek, D.Olszewska, K.Kurpiewska, M.Dziedzicka-Wasylewska, … K.Lewiński, (2012). Structural and thermodynamic studies of binding saturated fatty acids to bovine β-lactoglobulin. International Journal of Biological Macromolecules, 50, 1095–1102. doi:10.1016/j.ijbiomac.2012.03.002
36. A.Mensi, Y.Choiset, H.Rabesona, T.Haertlé, P.Borel, & J.M.Chobert, (2013). Interactions of β-Lactoglobulin variants A and B with vitamin A. Competitive binding of retinoids and carotenoids. Journal of Agricultural and Food Chemistry, 61, 4114–4119. doi:10.1021/jf400711d
37. D.Mercadante, L.D.Melton, G.E.Norris, T.S.Loo, M.A.Williams, R.C.Dobson, … G.B.Jameson, (2012). Bovine β-lactoglobulin is dimeric under imitative physiological conditions:Dissociation equilibrium and rate constants over the pH range of 2.5–7.5. Biophysical Journal, 103, 303–312. doi:10.1016/j.bpj.2012.05.041
38. B.R.Miller, T.D.McGee, J.M.Swails, N.Homeyer, H.Gohlke, & A.E.Roitberg, (2012). MMPBSA.py:An efficient program for end-state free energy calculations. Journal of Chemical Theory and Computation, 8, 3314–3321. doi:10.1021/ct300418h
39. G.M.Morris, R.Huey, W.Lindstrom, M.F.Sanner, R.K.Belew, D.S.Goodsell, … A.J.Olson, (2009). AutoDock4 and AutoDockTools4:Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30, 2785–2791. doi:10.1002/jcc.21256
40. S.Muresan, A.van der Bent, & F.A.de Wolf, (2001). Interaction of β-lactoglobulin with small hydrophobic ligands as monitored by fluorometry and equilibrium dialysis:Nonlinear quenching effects related to protein−protein association. Journal of Agricultural and Food Chemistry, 49, 2609–2618. doi:10.1021/jf0012188
41. S.Nagaoka, Y.Futamura, K.Miwa, T.Awano, K.Yamauchi, Y.Kanamaru, … T.Kuwata, (2001). Identification of novel hypocholesterolemic peptides derived from bovine milk β-lactoglobulin. Biochemical and Biophysical Research Communications, 281, 11–17. doi:10.1006/bbrc.2001.4298
42. H.Ohtomo, K.Fujiwara, & M.Ikeguchi, (2012). Important role of methionine 145 in dimerization of bovine β-lactoglobulin. Journal of Biochemistry, 151, 329–334. doi:10.1093/jb/mvr142
43. A.Onufriev, D.Bashford, & D.A.Case, (2004). Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins:Structure, Function, and Bioinformatics, 55, 383–394. doi:10.1002/prot.20033
44. M.D.Perez, L.Sanchez, P.Aranda, J.M.Ena, R.Oria, & M.Calvo, (1992). Effect of β-lactoglobulin on the activity of pregastric lipase. A possible role for this protein in ruminant milk. Biochimica et Biophysica Acta, 1123, 151–155. doi:10.1016/0005-2760(92)90105-5
45. G.N.Phillips, Jr (1990). Comparison of the dynamics of myoglobin in different crystal forms. Biophysical Journal, 57, 381–383. doi:10.1016/S0006-3495(90)82540-6
46. B.Y.Qin, M.C.Bewley, L.K.Creamer, H.M.Baker, E.N.Baker, & G.B.Jameson, (1998). Structural basis of the Tanford transition of bovine β-lactoglobulin. Biochemistry, 37, 14014–14023. doi:10.1021/bi981016t
47. B.Y.Qin, L.K.Creamer, E.N.Baker, & G.B.Jameson, (1998). 12-Bromododecanoic acid binds inside the calyx of bovine β-lactoglobulin. FEBS Letters, 438, 272–278. doi:10.1016/S0014-5793(98)01199-5
48. L.H.Riihimäki, M.J.Vainio, J.M.S.Heikura, K.H.Valkonen, V.T.Virtanen, & P.M.Vuorela, (2008). Binding of phenolic compounds and their derivatives to bovine and reindeer β-lactoglobulin. Journal of Agricultural and Food Chemistry, 56, 7721–7729. doi:10.1021/jf801120a
49. K.Sakurai, & Y.Goto, (2002). Manipulating monomer-dimer equilibrium of bovine β-lactoglobulin by amino acid substitution. Journal of Biological Chemistry, 277, 25735–25740. doi:10.1074/jbc.M203659200
50. R.Salomon-Ferrer, A.W.Götz, D.Poole, S.Le Grand, & R.C.Walker, (2013). Routine microsecond molecular dynamics simulations with AMBER-Part II:Particle mesh Ewald. Journal of Chemical Theory and Computation, 9, 3878–3888. doi:10.1021/ct200909j
51. L.Sawyer, (2003). β-Lactoglobulin, in advanced dairy chemistry. (P.F.Fox, & P.L.H.McSweeney, Trans., 3rd ed., pp. 319–386). New York:Kluwer Academic, Plenum Publishers.
52. L.Sawyer, & G.Kontopidis, (2000). The core lipocalin, bovine β-lactoglobulin. Biochimica et Biophysica Acta, 1482, 136–148. doi:10.1016/S0167-4838(00)00160-6
53. L.F.Sutton, & B.Alston-Mills, (2006). β-Lactoglobulin as a potential modulator of intestinal activity and morphology in neonatal piglets. The Anatomical Record Part A:Discoveries in Molecular, Cellular, and Evolutionary Biology, 288A, 601–608. doi:10.1002/ar.a.20327
54. S.K.Tripathi, R.Muttineni, & S.K.Singh, (2013). Extra precision docking, free energy calculation and molecular dynamics simulation studies of CDK2 inhibitors. Journal of Theoretical Biology, 334, 87–100. doi:10.1016/j.jtbi.2013.05.014
55. S.Uhrínová, M.H.Smith, G.B.Jameson, D.Uhrín, L.Sawyer, & P.N.Barlow, (2000). Structural changes accompanying pH-induced dissociation of the beta-lactoglobulin dimer. Biochemistry, 39, 3565–3574. doi:10.1021/bi992629o
56. W.F.Van Gunsteren, & H.J.C.Berendsen, (1977). Algorithms for macromolecular dynamics and constraint dynamics. Molecular Physics, 34, 1311–1327. doi:10.1080/00268977700102571
57. M.Verheul, J.S.Pedersen, S.P.Roefs, & K.G.de Kruif, (1999). Association behavior of native beta-lactoglobulin. Biopolymers, 49, 11–20. doi:10.1002/(SICI)1097-0282(199901)49:1<11::AID-BIP2>3.0.CO;2-1
58. J.Wang, T.Hou, & X.Xu, (2006). Recent advances in free energy calculations with a combination of molecular mechanics and continuum models. Current Computer Aided-Drug Design, 2, 287–306. doi:10.2174/157340906778226454
59. J.Wang, R.M.Wolf, J.W.Caldwell, P.A.Kollman, & D.A.Case, (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25, 1157–1174. doi:10.1002/jcc.20035
60. S.Y.Wu, M.D.Perez, P.Puyol, & L.Sawyer, (1999). β-Lactoglobulin binds palmitate within its central cavity. Journal of Biological Chemistry, 274, 170–174. doi:10.1074/jbc.274.1.170
61. M.C.Yang, H.H.Guan, M.Y.Liu, Y.H.Lin, J.M.Yang, W.L.Chen, … S.J.Mao (2008). Crystal structure of a secondary vitamin D3 binding site of milk beta-lactoglobulin. Proteins, 71, 1197–1210. doi:10.1002/prot.21811
62. M.C.Yang, N.C.Chen, C.J.Chen, C.Y.Wu, & S.J.Mao, (2009). Evidence for beta-lactoglobulin involvement in vitamin D transport in vivo–role of the gamma-turn (Leu-Pro-Met) of beta-lactoglobulin in vitamin D binding. FEBS Journal, 276, 2251–2265. doi:10.1111/j.1742-4658.2009.06953.x
63. R.Zorilla, L.Liang, G.Remondetto, & M.Subirade, (2011). Interaction of epigallocatechin- 3-gallate with β-lactoglobulin:Molecular characterization and biological implication. Dairy Science & Technology, 91, 629–644. doi:10.1007/s13594-011-0036-3