Effect of heat treatment on bovine β-lactoglobulin A, B, and C explored using thiol availability and fluorescence

Journal of Agricultural and Food Chemistry

Volumn 47, Issue 9, 1999, Pages 3617-3627

  Manderson, Gavin A ^a,b,c   Hardman, Michael J ^a   Creamer, Lawrence K ^b  

^a MASSEY UNIVERSITY   (New Zealand)

^b NEW ZEALAND DAIRY RESEARCH INSTITUTE   (New Zealand)

^c WISTAR INSTITUTE   (United States)

Author keywords

lactoglobulin variants; Aggregate formation; ANS fluorescence; Disulfide linked aggregates; DTNB; Thermal denaturation; Tryptophan fluorescence

Indexed keywords

5,5' DITHIOBIS(2 NITROBENZOIC ACID); 8 ANILINO 1 NAPHTHALENESULFONIC ACID; BETA LACTOGLOBULIN; ISOPROTEIN; LACTOGLOBULIN; MILK; THIOL; THIOL DERIVATIVE;

ANIMAL; ARTICLE; BINDING SITE; CATTLE; CHEMICAL ANALYSIS; CHEMISTRY; COW; DISULFIDE BOND; FLUORESCENCE; HEAT; HEAT TREATMENT; METHODOLOGY; NONHUMAN; SPECTROFLUOROMETRY; THERMODYNAMICS;

ANIMALS; CATTLE; DITHIONITROBENZOIC ACID; HEAT; LACTOGLOBULINS; PROTEIN ISOFORMS; SPECTROMETRY, FLUORESCENCE; SULFHYDRYL COMPOUNDS; THERMODYNAMICS;

ANIMALIA; BOS TAURUS; BOVINAE;

EID: 0032839589     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf990591g     Document Type: Article

References (50)

1. Arighi, C. N.; Rossi, J. P. F. C.; Delfino, J. M. Temperature-induced conformational transition of intestinal fatty acid binding protein enhancing ligand binding: a functional, spectroscopic, and molecular modeling study. Biochemistry 1998, 37, 16802-16814.
2. Bewley, M. C.; Qin, B. Y.; Jameson, G. B.; Sawyer, L.; Baker, E. N. β-Lactoglobulin and its variants: a three-dimensional structural perspective. In International Dairy Federation Special Issue 9702. Milk Protein Polymorphism; International Dairy Federation: Brussels, 1997; pp 100-109.
3. Brand, L.; Gohlke, J. R. Fluorescence probes for structure. Annu. Rev. Biochem. 1972, 41, 843-868.
4. Brittan, H.; Mudford, J. C.; Norris, G. E.; Kitson, T. M.; Hill, J. P. Labelling the free sulfhydryl group in β-lactoglobulin A, B and C. In International Dairy Federation Special Issue 9702. Milk Protein Polymorphism; International Dairy Federation: Brussels, 1997; pp 200-203.
5. Brownlow, S.; Morais Cabral, J. H.; Cooper, R.; Flower, D. R.; Yewdall, S. J.; Polikarpov, I.; North, A. C. T.; Sawyer, L. Bovine β-lactoglobulin at 1.8 Å resolution-still an enigmatic lipocalin. Structure 1997, 5, 481-495.
6. Cairoli, S.; Iametti, S.; Bonomi, F. Reversible and irreversible modifications of β-lactoglobulin upon exposure to heat. J. Protein Chem. 1994, 13, 347-354.
7. Cardamone, M.; Puri, N. Spectrofluorometric assessment of the surface hydrophobicity of proteins. Biochem. J. 1992, 282, 589-593.
8. Chen, Y.; Barkley, M. D. Towards understanding tryptophan fluorescence in proteins. Biochemistry 1998, 37, 9976-9982.
9. Cho, Y.; Batt, C. A.; Sawyer, L. Probing the retinol-binding site of bovine β-lactoglobulin. J. Biol. Chem. 1994, 269, 11102-11107.
10. Cowgill, R. W. Fluorescence and protein structure. XI: Fluorescence quenching by disulphide and sulphydryl groups. Biochim. Biophys. Acta 1967, 140, 37-44.
11. Creamer, L. K. Effect of sodium dodecyl sulfate and palmitic acid on the equilibrium unfolding of bovine β-lactoglobulin. Biochemistry 1995, 34, 7170-7176.
12. Eftink, M. R. Fluorescence techniques for studying protein structure. Methods Biochem. Anal. 1991, 35, 127-205.
13. Gasymov, O. K.; Abduragimov, A. R.; Yusifov, T. N.; Glasgow, B. J. Structural changes in human tear lipocalins associated with lipid binding. Biochim. Biophys. Acta 1998, 1388, 145-156.
14. Hambling, S. G.; McAlpine, A. S.; Sawyer, L. β-Lactoglobulin. In Advanced Dairy Chemistry-1 Proteins; Fox, P. F., Ed.; Elsevier Applied Science: London, 1992; pp 141-165.
15. Hayakawa, S.; Nakai, S. Relationships of hydrophobicity and net charge to the solubility of milk and soy proteins. J. Food Sci. 1985, 50, 486-491.
16. Hennecke, J.; Sillen, A.; Huber-Wunderlich, M.; Engelborghs, Y.; Glockohuber, R. Quenching of tryptophan fluorescence by the active-site disulfide bridge in the DsbA protein from Esherichia coli. Biochemistry 1997, 36, 6391-6400.
17. Hoffmann, M. A. M.; van Mil, P. J. J. M. Heat-induced aggregation of β-lactoglobulin: role of the free thiol group and disulfide bonds. J. Agric. Food Chem. 1997, 45, 2942-2948.
18. Iametti, S.; De Gregori, B.; Vecchio, G.; Bonomi, F. Modifications occur at different structural levels during the heat denaturation of β-lactoglobulin. Eur. J. Biochem. 1998, 237, 106-112.
19. Kirk, W.; Kurian, E.; Prendergast, F. Characterization of the sources of protein-ligand affinity: 1-sulfato-8-(1′)-anilinonaphthalene binding to intestinal fatty acid binding protein. Biophys. J. 1996, 70, 69-83.
20. Kuwajima, K. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins: Struct. Funct. Genet. 1989, 6, 87-103.
21. Kuwajima, K. The molten globule state of α-lactalbumin. FASEB J. 1996, 10, 102-109.
22. Lakowicz, J. R. Principles of Fluorescence Spectroscopy; Plenum Press: New York, 1983.
23. Laligant, A.; Dumay, E.; Valencia, C. C.; Cuq, J.-L.; Cheftel, J.-C. Surface hydrophobicity and aggregation of β-lactoglobulin heated near neutral pH. J. Agric. Food Chem. 1991, 39, 2147-2155.
24. Leatherbarrow, R. J. Enzfitter, a nonlinear regression data analysis program for the IBM PC; Biosoft: UK, 1987.
25. Luo, J.; Mathews, C. R.; Iwakura, M. Detection of a stable intermediate in the thermal unfolding of a cysteine-free form of dehydrofolate reductase from Escherichia coli. Biochemistry 1995, 34, 10669-10675.
26. Manderson, G. A. The effect of heat on the structure and aggregation behaviour of bovine β-lactoglobulins A, B and C. Ph.D. Thesis, Massey University, New Zealand, 1998.
27. Manderson, G.; Hardman, M. J.; Creamer, L. K. Thermal denaturation of β-lactoglobulin A, B, and C. J. Dairy Sci. 1995, 78 (Suppl. 1), 132.
28. Manderson, G. A.; Hardman, M. J.; Creamer, L. K. Spectroscopic examination of the heat-induced changes in β-lactoglobulin A, B and C. In International Dairy Federation Special Issue 9702. Milk Protein Polymorphism; International Dairy Federation: Brussels, 1997; pp 204-211.
29. Manderson, G. A.; Hardman, M. J.; Creamer, L. K. Effect of heat treatment on conformation and aggregation of β-lactoglobulin A, B, and C. J. Agric. Food Chem. 1998, 46, 5052-5061.
30. Manderson, G. A.; Creamer, L. K.; Hardman, M. J. Effect of heat treatment on the circular dichroism spectra of bovine β-lactoglobulin A, B, and C. J. Agric. Food Chem. 1999 (in press).
31. Matulis, D.; Lovrien, R. 1-Anilino-8-naphthalene sulfonate anion-protein binding depends primarily on ion pair formation. Biophys. J. 1998, 74, 422-429.
32. McKenzie, H. A. β-Lactoglobulins. In Milk Proteins. Chemistry and Molecular Biology; McKenzie, H. A., Ed.; Academic Press: New York, 1971; Vol. II, pp 257-330.
33. Mills, O. E. Effect of temperature on tryptophan fluorescence of β-lactoglobulin B. Biochim. Biophys. Acta 1976, 434, 324-332.
34. Mills, O. E.; Creamer, L. K. A conformational change in bovine β-lactoglobulin at low pH. Biochim. Biophys. Acta 1975, 379, 618-626.
35. Møller, R. E.; Stapelfeldt, H.; Skibsted, L. H. Thiol reactivity in pressure-unfolded β-lactoglobulin. Antioxidative properties and thermal refolding. J. Agric. Food Chem. 1998, 46, 425-430.
36. Morgan, F.; Léonil, J.; Mollé, D.; Bouhallab, S. Modification of bovine β-lactoglobulin by glycation in a powdered state or in an aqueous solution: effect on association behavior and protein conformation. J. Agric. Food Chem. 1999, 47, 83-91.
37. Mulvihill, D. M.; Donovan, M. Whey proteins and their thermal denaturation - a review. Irish J. Food Sci. Technol. 1987, 11, 43-75.
38. 13C-n.m.r. of the cyanylated β-lactoglobulins: evidence that Cys-121 provides the thiol group of β-lactoglobulins A and B. Biochem. J. 1994, 302, 511-516.
39. Phillips, N. I.; Jenness, R.; Kalan, E. B. Reactivity of sulfhydryls in several β-lactoglobulins. Arch. Biochem. Biophys. 1967, 120, 192-197.
40. Qi, X. L.; Brownlow, S.; Holt, C.; Sellers, P. Thermal denaturation of β-lactoglobulin: effect of protein concentration at pH 6.75 and 8.05. Biochim. Biophys. Acta 1995, 1248, 43-49.
41. Qi, X. L.; Holt, C.; McNulty, D.; Clarke, D. T.; Brownlow, S.; Jones, G. R. Effect of temperature on the secondary structure of β-lactoglobulin at pH 6.7, as determined by CD and IR spectroscopy: a test of the molten globule hypothesis. Biochem. J. 1997, 324, 341-346.
42. Qin, B. Y.; Creamer, L. K.; Baker, E. N.; Jameson, G. B. 12-Bromododecanoic acid binds inside the calyx of bovine β-lactoglobulin. FEBS Lett. 1998a, 438, 272-278.
43. Qin, B. Y.; Bewley, M. C.; Creamer, L. K.; Baker, H. M.; Baker, E. N.; Jameson, G. B. Structural basis of the Tanford transition of bovine β-lactoglobulin. Biochemistry 1998b, 37, 14014-14023.
44. Qin, B. Y.; Bewley, M. C.; Creamer, L. K.; Baker, E. N.; Jameson, G. B. Structural and functional differences of variants A and B of bovine β-lactoglobulin. Protein Sci. 1999, 8, 1-9.
45. Renard, D.; Lefebvre, J.; Griffin, M. C. A.; Griffin, W. G. Effects of pH and salt environment on the association of β-lactoglobulin revealed by intrinsic fluorescence studies. Int. J. Biol Macromol. 1998, 22, 41-49.
46. Sawyer, W. H.; Coulter, S. T.; Jenness, R. Role of sulfhydryl groups in the interaction of κ-casein and β-lactoglobulin. J. Dairy Sci. 1963, 46, 564-565.
47. Slavík, J. Anilinonaphthalene sulfonate as a probe of membrane composition and function. Biochim. Biophys. Acta 1982, 694, 1-25.
48. Stapelfeldt, H.; Petersen, P. H.; Kristiansen, K. R.; Qvist, K. B.; Skibsted, L. H. Effect of high hydrostatic pressure on the enzymic hydrolysis of β-lactoglobulin B by trypsin, thermolysin and pepsin. J. Dairy Res. 1996, 63, 111-118.
49. Stryer, L. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe for nonpoplar sites. J. Mol. Biol. 1966, 13, 482-495.
50. Wu, S. Y.; Pérez, M. D.; Puyol, P.; Sawyer. L. β-Lactoglobulin binds palmitate within its central cavity. J. Biol. Chem. 1999, 274, 170-174.