Characterization and in vitro digestibility of bovine β-lactoglobulin glycated with galactooligosaccharides

Journal of Agricultural and Food Chemistry

Volumn 55, Issue 19, 2007, Pages 7916-7925

  Sanz, María Luz ^a   Corzo Martínez, Marta ^b   Rastall, Robert A ^c   Olano, Agustín ^b   Moreno, F Javier ^b  

^a INSTITUTO DE QUÍMICA ORGÁNICA GENERAL   (Spain)

^b INSTITUTO DE FERMENTACIONES INDUSTRIALES CSIC   (Spain)

^c UNIVERSITY OF READING   (United Kingdom)

Author keywords

Lactoglobulin; Galactooligosaccharides; Gastrointestinal digestion; Maillard reaction; Prebiotic

Indexed keywords

GALACTOSE; LACTOGLOBULIN; OLIGOSACCHARIDE;

ANIMAL; ARTICLE; CATTLE; CHEMISTRY; DIGESTION; GLYCOSYLATION; IN VITRO STUDY; MASS SPECTROMETRY; METABOLISM;

ANIMALS; CATTLE; DIGESTION; GALACTOSE; GLYCOSYLATION; LACTOGLOBULINS; OLIGOSACCHARIDES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

BOVINAE; TETRA;

EID: 34948870766     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf071111l     Document Type: Article

References (57)

1. Steer, T.; Carpenter, H.; Tuohy, K.; Gibson, G. R. Perspectives on the role of the human gut microbiota and its modulation by pro- and prebiotics. Nutr. Res. Rev. 2000, 13, 229-254.
2. Madsen, K. L. The use of probiotics in gastrointestinal disease. Can. J. Gastroenterol. 2001, 15, 817-822.
3. Mountzouris, K. C.; McCartney, A. L.; Gibson, G. R. Intestinal microflora of human infants and current trends for its nutritional modulation. Br. J. Nutr. 2002, 87, 405-420.
4. Gibson, G. R.; Roberfroid, M. B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 1995, 125, 1401-1412.
5. Sanz, M. L.; Cote, G. L.; Gibson, G. R.; Rastall, R. A. Prebiotic properties of alternansucrase maltose-acceptor oligosaccharides. J. Agric. Food Chem. 2005, 53, 5911-5916.
6. Franck, A. Prebiptics stimulate calcium absorption: A review. Food Aust. 2005, 57, 530-532.
7. Snelling, A. M. Effects of probiotics on the gastrointestinal tract. Curr. Opin. Infect. Dis. 2005, 18, 420-426.
8. Lim, C. C.; Ferguson, L. R.; Tannock, G. W. Dietary fibres as "prebiotics": Implications for colorectal cancer. Mol. Nutr. Food Res. 2005, 49, 609-619.
9. Salminen, S.; Bouley, C.; Boutron-Ruault, M. C.; Cummings, J. H.; Franck, A.; Gibson, G. R.; Isolauri, E.; Moreau, M. C.; Roberfroid, M.; Rowland, I. Functional food science and gastrointestinal physiology and function. Br. J. Nutr. 1998, 80 (Suppl. 1), S147-S171.
10. Delzenne, N. M. Oligosaccharides: State of the art. Proc. Nutr. Soc. 2003, 62, 177-182.
11. Gibson, G. R.; Probert, H. M.; Van Loo, J.; Rastall, R. A.; Roberfroid, M. B. Dietary modulation of the human colonic microbiota: Updating the concept of prebiotics. Nutr. Res. Rev. 2004, 17, 259-275.
12. Haertle, T.; Chobert, J. M. Recent progress in processing of dairy proteins: A review. J. Food Biochem. 1999, 23, 367-407.
13. Kato, A. Industrial applications of Maillard-type protein-polysaccharide conjugates. Food Sci. Technol. Res. 2002, 8, 193-199.
14. Oliver, C. M.; Melton, L. D.; Stanley, R. A. Creating proteins with novel functionality via the Maillard reaction: A review. CRC Crit. Rev. Food Sci. Nutr. 2006, 46, 337-350.
15. Lee, K.; Erbersdobler, H. F. Balanced experiments in human volunteers with ε-fructoselysine and lysinoalanine. In Maillard Reactions in Chemistry, Food and Health; Labuza, T. P., Reineccius, G. A., Monnier, V. M., O'Brien, J., Baynes, J. W., Eds.; The Royal Society of Chemistry: Cambridge, U.K., 1994; pp 358-363.
16. Finot, P. A. Non enzymatic browning. In Proteins in Human Nutrition; Porter, J. W. G., Rolls, B. A., Eds.; Academic Press: London, 1973; pp 501-514.
17. Erbersdobler, H. F.; Faist, V. Metabolic transit of Amadori products. Nahrung 2001, 45, 177-181.
18. Faist, V.; Erbersdobler, H. F. Metabolic transit and in vivo effects of melanoidins and precursor compounds deriving from the Maillard reaction. Ann. Nutr. Metab. 2001, 45, 1-12.
19. Finot, P.-A. The absorption and metabolism of modified amino acids in processed foods. J. AOAC Int. 2005, 88, 894-903.
20. Dell'Aquila, C.; Ames, J. M.; Gibson, G. R.; Wynne, A. G. Fermentation of heated gluten systems by gut microflora. Eur. Food Res. Technol. 2003, 217, 382-386.
21. Tuohy, K. M.; Hinton, D. J. S.; Davies, S. J.; Crabbe, M. J. C.; Gibson, G. R.; Ames, J. M. Metabolism of Maillard reaction products by the human gut microbiota: Implications for health. Mol. Nutr. Food Res. 2006, 50, 847-857.
22. Nacka, F.; Chobert, J.-M.; Burova, T.; Leonil, J.; Haertle, T. Induction of new physicochemical and functional properties by the glycosylation of whey proteins. J. Protein Chem. 1998, 17, 495-503.
23. Morgan, F.; Leonil, J.; Molle, 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.
24. Chevalier, F.; Chobert, J. M.; Dalgalarrondo, M.; Choiset, Y.; Haertle, T. Maillard glycation of β-lactoglobulin induces conformation changes. Nahrung 2002, 46, 58-63.
25. Fenaille, F.; Morgan, F.; Parisod, V.; Tabet, J.-C.; Guy, P. A. Solid-state glycation of β-lactoglobulin monitored by electrospray ionisation mass spectrometry and gel electrophoresis techniques. Rapid Commun. Mass Spectrom. 2003, 17, 1483-1492.
26. Jimenez-Castano, L.; Villamiel, M.; Martin-Alvarez, P. J.; Olano, A.; Lopez-Fandino, R. Effect of the dry-heating conditions on the glycosylation of β-lactoglobulin with dextran through the Maillard reaction. Food Hydrocolloids 2005, 19, 831-837.
27. Anthony, J. C.; Merriman, T. N.; Heimbach, J. T. 90-Day oral (gavage) study in rats with galactooligosaccharides syrup. Food Chem. Toxicol. 2006, 44, 819-826.
28. Morales, V.; Sanz, M. L.; Olano, A.; Corzo, N. Rapid separation on activated charcoal of high oligosaccharides in honey. Chromatographia 2006, 64, 233-238.
29. Moreno, F. J.; Lopez-Fandino, R.; Olano, A. Characterization and functional properties of lactosyl caseinomacropeptide conjugates. J. Agric. Food Chem. 2002, 50, 5179-5184.
30. Resmini, P.; Pellegrino, L.; Batelli, G. Accurate quantification of furosine in milk and dairy products by a direct HPLC method. Ital. J. Food Sci. 1990, 2, 173-183.
31. McKellar, R. C. Development of off-flavors in ultra-high temperature and pasteurized milk as a function of proteolysis. J. Dairy Sci. 1981, 64, 2138-2145.
32. Ting, S. V.; Rouseff, R. L. Undesirable substances formed during processing and storage. In Citrus Fruit and Their Products. Analysis and Technology; Tannenbaum, S. R., Walstra, P., Eds.; Marcel Dekker Inc.: New York, 1986; pp 175-182.
33. Zacharius, R. M.; Zell, T. E.; Morrison, J. H.; Woodlock, J. J. Glycoprotein staining following electrophoresis on acrylamide gels. Anal. Biochem. 1969, 30, 148-152.
34. Casal, E.; Montilla, A.; Moreno, F. J.; Olano, A.; Corzo, N. Use of chitosan for selective removal of β-lactoglobulin from whey. J. Dairy Sci. 2006, 89, 1384-1389.
35. Moreno, F. J.; Mellon, F. A.; Wickham, M. S. J.; Bottrill, A. R.; Mills, E. N. C Stability of the major allergen Brazil nut 2S albumin (Ber e 1) to physiologically-relevant in vitro gastrointestinal digestion. FEBS J. 2005, 272, 341-352.
36. Board of Trustees. Simulated Gastric Fluid, TS. In The United States Pharmacopeia 23, The National Formulary 18; United States Pharmacopeial Convention, Inc.: Rockville, MD, 1995; pp 2053.
37. Moreno, F. J.; Jenkins, J. A.; Mellon, F. A.; Rigby, N. M.; Robertson, J. A.; Wellner, N.; Mills, E. N. C. Mass spectrometry and structural characterization of 2S albumin isoforms from Brazil nuts (Berthollelia excelsa). Biochim. Biophys. Acta 2004, 1698, 175-186.
38. Goulas, A. K.; Grandison, A. S.; Rastall, R. A. Fractionation of oligosaccharides by nanofiltration. J. Sci. Food Agric. 2003, 83, 675-680.
39. Fenaille, F.; Campos-Gimenez, E.; Guy, P. A.; Schmitt, C.; Morgan, F. Monitoring of β-lactoglobulin dry-state glycation using various analytical techniques. Anal. Biochem. 2003, 320, 144-148.
40. Chevalier, F.; Chobert, J. M.; Dalgalarrondo, M.; Haertle, T. Characterization of the Maillard reaction products of β-lactoglobulin glucosylated in mild conditions. J. Food Biochem. 2001, 25, 33-55.
41. Jimenez-Castano, L.; Lopez-Fandino, R.; Olano, A.; Villamiel, M. Study on β-lactoglobulin glycosylation with dextran: Effect on solubility and heat stability. Food Chem. 2005, 93, 689-695.
42. Bunn, H. F.; Shapiro, R.; McManus, M.; Garrick, L.; McDonald, M. J.; Gallop, P. M.; Gabbay, K. H. Structural heterogeneity of human haemoglobin A due to nonenzymatic glycosylation. J. Biol. Chem. 1979, 254, 3892-3898.
43. Leonil, J.; Molle, D.; Fauquant, J.; Maubois, J. L.; Pearce, R. J.; Bouhallab, S. Characterization by ionization mass spectrometry of lactosyl β-lactoglobulin conjugates formed during heat treatment of milk and whey and identification of one lactose-binding site. J. Dairy Sci. 1997, 80, 2270-2281.
44. Broersen, K.; Voragen, A. G. J.; Hamer, R. J.; de Jongh, H. H. J. Glycoforms of β-lactoglobulin with improved thermostability and preserved structural packing. Biotechnol. Bioeng. 2004, 86, 78-87.
45. Van Teeffelen, A. M. M.; Broersen, K.; De Jongh, H. H. J. Glucosylation of β-lactoglobulin lowers the heat capacity change of unfolding: A unique way to affect protein thermodynamics. Protein Sci. 2005, 14, 2187-2194.
46. Astwood, J. D.; Leach, J. N.; Fuchs, R. L. Stability of food allergens to digestion in vitro. Nat. Biotechnol. 1996, 14, 1269-1273.
47. Schmidt, D. G.; Meijer, R. J.; Slangen, C. J.; van Beresteijn, E. C. Raising the pH of the pepsin-catalyzed hydrolysis of bovine whey proteins increases the antigenicity of the hydrolysates. Clin. Exp. Allergy 1995, 25, 1007-1017.
48. Chobert, J. M.; Briand, L.; Dufour, E.; Dib, R.; Dalgalarrondo, M.; Haertle, T. How to increase β-lactoglobulin susceptibility to peptic hydrolysis. J. Food Biochem. 1997, 20, 439-462.
49. Kitabatake, N.; Kinekawa, Y.-I. Digestibility of bovine milk whey protein and β-lactoglobulin in vitro and in vivo. J. Agric. Food Chem. 1998, 46, 4917-4923.
50. Reddy, I. M.; Kella, N. K. D.; Kinsella, J. E. Structural and conformational basis of the resistance of β-lactoglobulin to peptic and chymotryptic digestion. J. Agric. Food Chem. 1988, 36, 737-741.
51. Dalgalarrondo, M.; Dufour, E.; Chobert, J.-M.; Bertrand-Harb, C.; Haertle, T. Proteolysis of β-lactoglobulin and β-casein by pepsin in ethanolic media. Int. Dairy J. 1995, 5, 1-14.
52. Morgan, F.; Molle, D.; Henry, G.; Vénien, A.; Leonil, J.; Peltre, G.; Levieux, D.; Maubois, J.-L.; Bouhallab, S. Glycation of bovine β-Lactoglobulin: Effect on the protein structure. Int. J. Food Sci. Technol. 1999, 34, 429-435.
53. Macfarlane, G. T.; Gibson, G. R. Microbiological aspects of short chain fatty acid production in the large bowel. In Physiological and Clinical Aspects of Short Chain Fatty Acid Metabolism; Cummings, J. H., Rombeau, J. L., Sakata, T., Eds.; Cambridge University Press: Cambridge, U.K., 1995; pp 87-105.
54. Henle, T.; Klostermeyer, H. The reactivity of the individual protein-bound lysine residues of β-casein al during the initial stages of the Maillard-reaction. In International Dairy Federation Special Issue 9303. Protein and fat globule modifications by heat treatment, homogenization and other technological means for high quality dairy products; International Dairy Federation: Brussels, 1993; pp 183-189.
55. Morgan, F.; Leonil, J.; Molle, D.; Bouhallab, S. Nonenzymatic lactosylation of bovine β-lactoglobulin under mild heat treatment leads to structural heterogeneity of the glycoforms. Biochem. Biophys. Res. Commun. 1997, 236, 413-417.
56. Lapolla, A.; Fedele, D.; Martano, L.; Arico, N. C.; Garbeglio, M.; Traldi, P.; Seraglia, R.; Favretto, D. Advanced glycation end products: A highly complex set of biologically relevant compounds detected by mass spectrometry. J. Mass Spectrom. 2001, 36, 370-378.
57. Lapolla, A.; Fedele, D.; Reitano, R.; Arico, N. C.; Seraglia, R.; Traldi, P.; Marotta, E.; Tonani, R. Enzymatic digestion and mass spectrometry in the study of advanced glycation end products/peptides. J. Am. Soc. Mass Spectrom. 2004, 15, 496-509.