Differences in heat stability and ligand binding among β-lactoglobulin genetic variants A, B and C using 1H NMR and fluorescence quenching

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 6, 2014, Pages 1083-1093

  Keppler, Julia K ^a   Sönnichsen, Frank D ^a   Lorenzen, Peter Christian ^b   Schwarz, Karin ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

Author keywords

Epigallocatechingallate binding; Fluorescence quenching; Genetic variant; Protein heat stability; Protein ligand interaction; Retinol binding; Lactoglobulin

Indexed keywords

BETA LACTOGLOBULIN; EPIGALLOCATECHIN GALLATE; HISTIDINE; PHENYLALANINE; RETINOL; TYROSINE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; FLUORESCENCE QUENCHING; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN UNFOLDING; PROTON NUCLEAR MAGNETIC RESONANCE; THERMOSTABILITY;

EPIGALLOCATECHINGALLATE BINDING; FLUORESCENCE QUENCHING; GENETIC VARIANT; PROTEIN HEAT STABILITY; PROTEIN-LIGAND INTERACTION; RETINOL BINDING; Β-LACTOGLOBULIN;

ANIMALS; BINDING SITES; CATECHIN; CATTLE; CIRCULAR DICHROISM; KINETICS; LACTOGLOBULINS; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE; VITAMIN A;

EID: 84898606059     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.02.007     Document Type: Article

References (76)

1. J.J. Basch, and S.N. Timasheff Hydrogen ion equilibria of the genetic variants of bovine β-lactoglobulin Arch. Biochem. Biophys. 118 1967 37 47 (http://www.sciencedirect.com/science/article/pii/0003986167902755)
2. C. Barbana, M.D. Pérez, L. Sánchez, M. Dalgalarrondo, J.M. Chobert, T. Haertlé, and M. Calvo Interaction of bovine [alpha]-lactalbumin with fatty acids as determined by partition equilibrium and fluorescence spectroscopy Int. Dairy J. 16 2006 18 25 http://www.sciencedirect. com/science/article/B6T7C-4G82XY9-2/2/464371ed5495711e6611bcb9f06bedb9 (Pubitemid 41531147)
3. M. Collini, L. D'Alfonso, H. Molinari, L. Ragona, M. Catalano, and G. Baldini Competitive binding of fatty acids and the fluorescent probe 1-8-anilinonaphthalene sulfonate to bovine beta-lactoglobulin Protein Sci. 12 2003 1596 1603 (Pubitemid 36910040)
4. A. Mensi, Y. Choiset, H. Rabesona, T. Haertlé, P. Borel, and J.-M. Chobert Interactions of β-lactoglobulin variants A and B with vitamin A. Competitive binding of retinoids and carotenoids J. Agric. Food Chem. 61 2013 4114 4119
5. S. Muresan, A. van der Bent, and F.A. de Wolf Interaction of β-lactoglobulin with small hydrophobic ligands as monitored by fluorometry and equilibrium dialysis: nonlinear quenching effects related to protein-protein association J. Agric. Food Chem. 49 2001 2609 2618 10.1021/jf0012188 (Pubitemid 32843298)
6. J.K. Keppler, T. Koudelka, K. Palani, M.C. Stuhldreier, F. Temps, A. Tholey, and K. Schwarz Characterization of the covalent binding of allyl isothiocyanate to β-lactoglobulin by fluorescence quenching, equilibrium measurement, and mass spectrometry J Biomol Struct Dyn 2013 10.1080/07391102. 2013.809605
7. X. Wu, R. Dey, H.U. Wu, Z. Liu, Q. He, and X. Zeng Studies on the interaction of -epigallocatechin-3-gallate from green tea with bovine β-lactoglobulin by spectroscopic methods and docking Int. J. Dairy Technol. 66 2012//2013 (no//7-13)
8. R. Zorilla, L. Liang, G. Remondetto, and M. Subirade Interaction of epigallocatechin-3-gallate with β-lactoglobulin: molecular characterization and biological implication Dairy Sci. Technol. 91 2011 629 644
9. L.H. Riihimäki, M.J. Vainio, J.M.S. Heikura, K.H. Valkonen, V.T. Virtanen, and P.M. Vuorela Binding of phenolic compounds and their derivatives to bovine and reindeer β-lactoglobulin J. Agric. Food Chem. 56 2008 7721 7729 10.1021/jf801120a
10. S. Rachagani, I.D. Gupta, N. Gupta, and S.C. Gupta Genotyping of beta-lactoglobulin gene by PCR-RFLP in Sahiwal and Tharparkar cattle breeds BMC Genet. 7 2006 31
11. E.B. Kalan, R. Greenberg, and M. Walter Studies on β-lactoglobulins A, B, and C. I. Comparison of chemical properties Biochemistry 4 1965 991 997
12. G.A. Manderson, L.K. Creamer, and M.J. Hardman Effect of heat treatment on the circular dichroism spectra of bovine beta-lactoglobulin A, B, and C J. Agric. Food Chem. 47 1999 4557 4567
13. G.A. Manderson, M.J. Hardman, and L.K. Creamer Effect of heat treatment on bovine β-lactoglobulin A, B, and C explored using thiol availability and fluorescence J. Agric. Food Chem. 47 1999 3617 3627 (Pubitemid 29449478)
14. G.A. Manderson, M.J. Hardman, and L.K. Creamer Effect of heat treatment on the conformation and aggregation of β-lactoglobulin A, B, and C J. Agric. Food Chem. 46 1998 5052 5061 (Pubitemid 128488257)
15. J.F. Bikker, S.G. Anema, Y. Li, and J.P. Hill Rheological properties of acid gels prepared from heated milk fortified with whey protein mixtures containing the A, B and C variants of β-lactoglobulin Int. Dairy J. 10 2000 723 732 (http://www.sciencedirect.com/science/article/pii/S0958694600000960) (Pubitemid 32169835)
16. S.R. Euston, R.L. Hirst, and J.P. Hill The emulsifying properties of β-lactoglobulin genetic variants A, B and C Colloids Surf. B: Biointerfaces 12 1999 193 202 (http://www.sciencedirect.com/science/article/pii/ S0927776598000745) (Pubitemid 29073753)
17. L.K. Creamer, H.C. Nilsson, M.A. Paulsson, C.J. Coker, J.P. Hill, and R. Jiménez-Flores Effect of genetic variation on the tryptic hydrolysis of bovine beta-lactoglobulin A, B, and C J. Dairy Sci. 87 2004 4023 4032 (Pubitemid 39606233)
18. M. Bello, M.d.C. Portillo-Téllez, and E. García- Hernández Energetics of ligand recognition and self-association of bovine β-lactoglobulin: differences between variants A and B Biochemistry 50 2011 151 161
19. A. Divsalar, A.A. Saboury, H. Mansoori-Torshizi, and A.A. Moosavi-Movahedi Binding properties of a new anti-tumor component (2,2′-bipyridin octylglycinato Pd(II) nitrate) with bovine beta-lactoglobulin-A and -B J. Biomol. Struct. Dyn. 25 2007 173 182 (Pubitemid 47454506)
20. T. Konuma, Y.-H. Lee, Y. Goto, and K. Sakurai Principal component analysis of chemical shift perturbation data of a multiple-ligand-binding system for elucidation of respective binding mechanism Proteins 81 2013 107 118
21. J.-L. Maubois, J. Fauquant, M.H. Famelart, F. Caussin, Milk microfiltrate, a convenient starting material for fractionation of whey proteins and derivatives, in: G. Andersen, 2.M. International Whey Conference 3 (Eds.), The importance of whey and whey components in food and nutrition. Proceedings of the 3rd International Whey Conference Munich 2001, Behr's Verlag, Hamburg, 2001, pp. 59-72.
22. I. Clawin-Rädecker, C. Kiesner, and E. Schlimme Analyse der säurelöslichen Gehalte von α-Lactalbumin, β-Lactoglobulin, Serumalbumin und der Immunglobulinfraktion in pasteurisierter Milch Kiel. Meeresforsch. Forsch. 2000 323 334
23. J.J. Kehoe, A. Brodkorb, D. Mollé, E. Yokoyama, M.-H. Famelart, S. Bouhallab, E.R. Morris, and T. Croguennec Determination of exposed sulfhydryl groups in heated β-lactoglobulin A using IAEDANS and mass spectrometry J. Agric. Food Chem. 55 2007 7107 7113 (Pubitemid 47338953)
24. K. Rade-Kukic, C. Schmitt, and H.M. Rawel Formation of conjugates between [beta]-lactoglobulin and allyl isothiocyanate: effect on protein heat aggregation, foaming and emulsifying properties. Food Colloids 2010: On the Road from Interfaces to Consumers Food Hydrocoll. 25 2011 694 706 (http://www.sciencedirect.com/science/article/pii/S0268005X10002006)
25. A. Shaka, J. Keeler, T. Frenkiel, and R. Freeman An improved sequence for broadband decoupling: WALTZ-16 J. Magn. Reson. 52 1969 335 338
26. U. Cogan, M. Kopelman, S. Mokady, and M. Shinitzky Binding affinities of retinol and related compounds to retinol binding proteins Eur. J. Biochem. 65 1976 71 78 10.1111/j.1432-1033.1976.tb10390.x
27. A. Shpigelman, Y. Cohen, and Y.D. Livney Thermally-induced β-lactoglobulin-EGCG nanovehicles: loading, stability, sensory and digestive-release study Food Hydrocoll. 29 2012 57 67 (http://www.sciencedirect. com/science/article/pii/S0268005X12000288)
28. A. Shpigelman, G. Israeli, and Y.D. Livney Thermally-induced protein-polyphenol co-assemblies: beta lactoglobulin-based nanocomplexes as protective nanovehicles for EGCG Food Hydrocoll. 24 2011 735 743 (http://www.sciencedirect.com/science/article/B6VP9-4YT6D9V-1/2/ 4ca30bb97971a654401eb48d0f14cb35)
29. M.C. Bewley, E.N. Baker, B.Y. Qin, G.B. Jameson, and L. Sawyer Bovine beta-lactoglobulin and its variants: a three-dimensional structural perspective Int. Dairy Fed. 1997 100 109
30. G.A. Manderson, L.K. Creamer, and M.J. Hardman Effect of heat treatment on the circular dichroism spectra of bovine β-lactoglobulin A, B, and C J. Agric. Food Chem. 47 1999 4557 4567
31. F. Chevalier, J.-M. Chobert, Y. Popineau, M.G. Nicolas, and T. Haertlé Improvement of functional properties of β-lactoglobulin glycated through the Maillard reaction is related to the nature of the sugar Int. Dairy J. 11 2001 145 152 (http://www.sciencedirect.com/science/article/pii/ S0958694601000401) (Pubitemid 32682566)
32. Z. Saadati, and A.-K. Bordbar Stability of β-lactoglobulin A in the presence of sugar osmolytes estimated from their guanidinium chloride-induced transition curves Protein J. 27 2008 455 460
33. K. Sakurai, and Y. Goto Dynamics and mechanism of the Tanford transition of bovine beta-lactoglobulin studied using heteronuclear NMR spectroscopy J. Mol. Biol. 356 2006 483 496 (Pubitemid 43099985)
34. S. Uhrínová, D. Uhrín, H. Denton, M. Smith, L. Sawyer, and P. Barlow Complete assignment of 1H, 13C and 15N chemical shifts for bovine β-lactoglobulin: secondary structure and topology of the native state is retained in a partially unfolded form J. Biomol. NMR 12 1998 89 107 10.1023/A%3A1008268528695 (Pubitemid 128512836)
35. L. Ragona, F. Pusterla, L. Zetta, H.L. Monaco, and H. Molinari Identification of a conserved hydrophobic cluster in partially folded bovine β-lactoglobulin at pH 2 Fold. Des. 2 1997 281 290 (http://www. sciencedirect.com/science/article/pii/S1359027897000394) (Pubitemid 127740550)
36. H. Molinari, L. Ragona, L. Varani, G. Musco, R. Consonni, L. Zetta, and H.L. Monaco Partially folded structure of monomeric bovine beta-lactoglobulin FEBS Lett. 381 1996 237 243 (Pubitemid 26080343)
37. T. Considine, H.A. Patel, S.G. Anema, H. Singh, and L.K. Creamer Interactions of milk proteins during heat and high hydrostatic pressure treatments A Review Innovative Food Science & Emerging Technologies 8 2007 1 23 (http://www.sciencedirect.com/science/article/pii/S1466856406000671) (Pubitemid 46217251)
38. 1H NMR Study J. Agric. Food Chem. 46 1998 1805 1813 (Pubitemid 128492919)
39. G. YuV, and V.P. Kutyshenko Differences in the processes of beta-lactoglobulin cold and heat denaturations Biophys. J. 67 1994 356 363
40. J.P. Hill, M.J. Boland, L.K. Creamer, A.G. Skelte, D.E. Otter, G.R. Paterson, R. Lowe, R.L. Motion, and W.C. Thresher Effect of the bovine β-lactoglobulin phenotype on the properties of β-lactoglobulin, milk composition, and dairy products ACS Symposium Series, Macromolecular Interactions in Food Technology 1996 American Chemical Society 281 294 (Pubitemid 126441643)
41. G.A. Manderson, M.J. Hardman, and L.K. Creamer Effect of heat treatment on the conformation and aggregation of β-lactoglobulin A, B, and C J. Agric. Food Chem. 46 1998 5052 5061 (Pubitemid 128488257)
42. B.Y. Qin, M.C. Bewley, L.K. Creamer, E.N. Baker, and G.B. Jameson Functional implications of structural differences between variants A and B of bovine beta-lactoglobulin Protein Sci. 8 1999 75 83 (Pubitemid 29035520)
43. J.I. Boye, C.-Y. Ma, and A.A. Ismail Thermal denaturation and gelation characteristics of β-lactoglobulin genetic variants ACS Symposium Series, Functional Properties of Proteins and Lipids 1998 American Chemical Society 168 183 (Pubitemid 128432719)
44. G.I. Imafidon, K.F. Ng-Kwai-Hang, V.R. Harwalkar, and C.-Y. Ma Differential scanning calorimetric study of different genetic variants of β-lactoglobulin J. Dairy Sci. 74 1991 2416 2422 (http://linkinghub. elsevier.com/retrieve/pii/S0022030291784166?showall=true)
45. M.M. Botelho, V.L. Valente-Mesquita, K.M.G. Oliveira, I. Polikarpov, and S.T. Ferreira Pressure denaturation of β-lactoglobulin Eur. J. Biochem. 267 2000 2235 2241
46. G. Gutiérrez-Magdaleno, M. Bello, M.C. Portillo-Téllez, A. Rodríguez-Romero, and E. García-Hernández Ligand binding and self-association cooperativity of β-lactoglobulin J. Mol. Recognit. 26 2013 67 75
47. P.R. Majhi, R.R. Ganta, R.P. Vanam, E. Seyrek, K. Giger, and P.L. Dubin Electrostatically driven protein aggregation: β-lactoglobulin at low ionic strength Langmuir 22 2006 9150 9159 (Pubitemid 44818499)
48. R. Bauer, S. Hansen, and L. ∅gendal Detection of intermediate oligomers, important for the formation of heat aggregates of β-lactoglobulin Int. Dairy J. 8 1998 105 112 (http://www.sciencedirect.com/ science/article/pii/S0958694698000272) (Pubitemid 28434029)
49. J.S. Mounsey Heat-Induced Denaturation/Aggregation of -Lactoglobulin as Affected by N-Ethylmaleimide, NaCl, CaCl2 and pH 1 2007 18 23 (http://medwelljournals.com/abstract/?doi=rjdsci.2007.18.23)
50. D. Renard, J. Lefebvre, M.C.A. Griffin, and W.G. Griffin Effects of pH and salt environment on the association of β-lactoglobulin revealed by intrinsic fluorescence studies Int. J. Biol. Macromol. 22 1998 41 49 (http://www.sciencedirect.com/science/article/pii/S014181309700086X) (Pubitemid 28073619)
51. S. Brownlow, J.H. Morais Cabral, R. Cooper, D.R. Flower, S.J. Yewdall, I. Polikarpov, A.C. North, and L. Sawyer Bovine beta-lactoglobulin at 1.8 A resolution - still an enigmatic lipocalin Structure 5 1997 481 495 (Pubitemid 27191225)
52. J. Yang, J.R. Powers, S. Clark, A.K. Dunker, and B.G. Swanson Hydrophobic probe binding of beta-lactoglobulin in the native and molten globule state induced by high pressure as affected by pH, KIO(3) and N-ethylmaleimide J. Agric. Food Chem. 50 2002 5207 5214 (Pubitemid 34925114)
53. G. Kontopidis, C. Holt, and L. Sawyer The ligand-binding site of bovine [beta]-lactoglobulin: evidence for a function J. Mol. Biol. 318 2002 1043 1055 (http://www.sciencedirect.com/science/article/B6WK7-45PMC6P-C/2/ baa80ac18bc08ba8977108e1d66aOdb8) (Pubitemid 35007367)
54. H.L. Monaco, G. Zanotti, P. Spadon, M. Bolognesi, L. Sawyer, and E.E. Eliopoulos Crystal structure of the trigonal form of bovine beta-lactoglobulin and of its complex with retinol at 2.5 A resolution J. Mol. Biol. 197 1987 695 706
55. D.C. Lange, R. Kothari, R.C. Patel, and S.C. Patel Retinol and retinoic acid bind to a surface cleft in bovine β-lactoglobulin: a method of binding site determination using fluorescence resonance energy transfer Biophys. Chem. 74 1998 45 51 (http://www.sciencedirect.com/science/article/pii/ S0301462298001641) (Pubitemid 28380350)
56. C.Y. Song, W.L. Chen, M.C. Yang, J.P. Huang, and S.J. Mao Epitope mapping of a monoclonal antibody specific to bovine dry milk. Involvement of residues 66-76 of strand D in thermal denatured beta-lactoglobulin J. Biol. Chem. 280 2005 3574 3582 (Pubitemid 40223823)
57. S.H. Mousavi, A.-K. Bordbar, and T. Haertlé Changes in structure and in interactions of heat-treated bovine beta-lactoglobulin Protein Pept. Lett. 15 2008 818 825
58. B.Y. Qin, M.C. Bewley, L.K. Creamer, H.M. Baker, E.N. Baker, and G.B. Jameson Structural basis of the Tanford transition of bovine beta-lactoglobulin Biochemistry 37 1998 14014 14023 (Pubitemid 28471234)
59. Y. Katakura, M. Totsuka, A. Ametani, and S. Kaminogawa Tryptophan-19 of beta-lactoglobulin, the only residue completely conserved in the lipocalin superfamily, is not essential for binding retinol, but relevant to stabilizing bound retinol and maintaining its structure Biochim. Biophys. Acta 1207 1994 58 67
60. E. Dufour, C. Genot, and T. Haertlé [Beta]-lactoglobulin binding properties during its folding changes studied by fluorescence spectroscopy Biochim. Biophys. Acta Protein Struct. Mol. Enzymol. 1205 1994 105 112 (http://www.sciencedirect.com/science/article/B6T21-47RSCK9-CW/2/ 7caacd69c2aaf7fc8cc02f70f054d7ac)
61. C.D. Kanakis, I. Hasni, P. Bourassa, P.A. Tarantilis, M.G. Polissiou, and H.-A. Tajmir-Riahi Milk β-lactoglobulin complexes with tea polyphenols Food Chem. 127 2011 1046 1055 (http://www.sciencedirect.com/science/article/pii/ S0308814611001828)
62. T. Konuma, K. Sakurai, and Y. Goto Promiscuous binding of ligands by β-lactoglobulin involves hydrophobic interactions and plasticity J. Mol. Biol. 368 2007 209 218 (http://www.sciencedirect.com/science/article/pii/ S0022283607001544) (Pubitemid 46441219)
63. M.C. Bohin, J.-P. Vincken, H.T.W.M. van der Hijden, and H. Gruppen Efficacy of food proteins as carriers for flavonoids J. Agric. Food Chem. 60 2012 4136 4143
64. K. Nagy, M.-C. Courtet-Compondu, G. Williamson, S. Rezzi, M. Kussmann, and A. Rytz Non-covalent binding of proteins to polyphenols correlates with their amino acid sequence Food Chem. 132 2012 1333 1339 (http://www. sciencedirect.com/science/article/pii/S0308814611017171)
65. B. Li, W. Du, J. Jin, and Q. Du Preservation of (-)-epigallocatechin-3- gallate antioxidant properties loaded in heat treated β-lactoglobulin nanoparticles J. Agric. Food Chem. 60 2012 3477 3484
66. M. Stojadinovic, J. Radosavljevic, J. Ognjenovic, J. Vesic, I. Prodic, D. Stanic-Vucinic, and T. Cirkovic Velickovic Binding affinity between dietary polyphenols and beta-lactoglobulin negatively correlates with the protein susceptibility to digestion and total antioxidant activity of complexes formed Food Chem. 136 2013 1263 1271
67. S. Cairoli, S. Iametti, and F. Bonomi Reversible and irreversible modifications of beta-lactoglobulin upon exposure to heat J. Protein Chem. 13 1994 347 354 (Pubitemid 24206334)
68. S. Iametti, B. de Gregori, G. Vecchio, and F. Bonomi Modifications occur at different structural levels during the heat denaturation of β-lactoglobulin Eur. J. Biochem. 237 1996 106 112 (Pubitemid 26110279)
69. R. Zorilla, L. Liang, G. Remondetto, and M. Subirade Interaction of epigallocatechin-3-gallate with β-lactoglobulin: molecular characterization and biological implication Dairy Sci. Technol. 91 2011 629 644
70. L. Tavel, C. Moreau, S. Bouhallab, E.C.Y. Li-Chan, and E. Guichard Interactions between aroma compounds and [beta]-lactoglobulin in the heat-induced molten globule state Food Chem. 119 2010 1550 1556 (http://www.sciencedirect.com/science/article/B6T6R-4X7240M-8/2/ f5367e760485cc2e7a86cd61d9ca9a11)
71. D. McPhail, and C. Holt Effect of anions on the denaturation and aggregation of beta Lactoglobulin as measured by differential scannind microcalorimetry Int. J. Food Sci. Technol. 34 1999 477 481 (Pubitemid 129513180)
72. B. Rullier, N. Novales, A. Bruno, and A.V. Monique Effect of protein aggregates on foaming properties of β-lactoglobulin Colloids Surf. A Physicochem. Eng. Asp. 330 2008 96 102
73. N. Mahmoudi, S. Mehalebi, T. Nicolai, D. Durand, and A. Riaublanc Light-scattering study of the structure of aggregates and gels formed by heat-denatured whey protein isolate and β-lactoglobulin at neutral pH J. Agric. Food Chem. 55 2007 3104 3111 (Pubitemid 46668324)
74. J.K. Keppler, M.C. Stuhldreier, F. Temps, and K. Schwarz Influence of mathematical models and correction factors on binding results of polyphenols and retinol with β-lactoglobulin measured with fluorescence quenching Food Biophys. 9 2014 10.1007/s11483-013-9328-x
75. G. Panick, R. Malessa, and D. Winter Differences between the pressure- and temperature-induced denaturation and aggregation of beta-lactoglobulin A, B, and AB monitored by FT-IR spectroscopy and small-angle X-ray scattering Biochemistry 38 1999
76. K. Sakurai, T. Konuma, M. Yagi, and Y. Goto Structural dynamics and folding of β-lactoglobulin probed by heteronuclear NMR: Recent Advances in Biochemistry, Biophysics and Molecular Biology Biochimica et Biophysica Acta (BBA) - General Subjects 1790 2009 527 537