Effect of glycation on the gastrointestinal digestibility and immunoreactivity of bovine β-lactoglobulin

International Dairy Journal

Volumn 20, Issue 11, 2010, Pages 742-752

  Corzo Martínez, Marta ^a   Soria, Ana Cristina ^a   Belloque, Josefina ^a   Villamiel, Mar ^a   Moreno, F Javier ^a  

^a INSTITUTO DE FERMENTACIONES INDUSTRIALES CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGENICITY; GASTROINTESTINAL DIGESTION; GLYCATION; IMMUNOREACTIVITIES; LACTOGLOBULIN; MAILLARD; MAILLARD REACTION; MASKING EFFECT; PROTEIN AGGREGATION; TAGATOSE;

CARBOHYDRATES; CHEMICAL REACTIONS; GLUCOSE;

PROTEINS;

BOVINAE;

EID: 77955510256     PISSN: 09586946     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.idairyj.2010.04.002     Document Type: Article

References (64)

1. Adams S.L., Barnett D., Walsh B.J., Pearce R.J., Hill D.J., Howden M.E.H. Human IgE-binding synthetic peptides of bovine β-lactoglobulin and α-lactalbumin. In vitro cross-reactivity of the allergens. Immunology and Cell Biology 1991, 69:191-197.
2. Aoki T., Iskandar S., Yoshida T., Takahashi K., Hattori M. Reduced immunogenicity of beta-lactoglobulin by conjugating with chitosan. Bioscience Biotechnology and Biochemistry 2006, 70:2349-2356.
3. Arita K., Babiker E.E., Azakami H., Kato A. Effect of chemical and genetic attachment of polysaccharides to proteins on the production of IgG and IgE. Journal of Agricultural and Food Chemistry 2001, 49:2030-2036.
4. Asselin J., Hébert J., Amiot J. Effects of in vitro proteolysis on the allergenicity of major whey proteins. Journal of Food Science 2006, 54:1031-1036.
5. Ball G., Shelton M.J., Walth B.J., Hill D.J., Hosking C.S., Howden M.E.H. A major continuous allergenic epitope of bovine α-lactoglobulin recognized by human IgE binding. Clinical and Experimental Allergy 1994, 24:758-764.
6. Beyer K., Morrow E., Li X.-M., Bardina L., Bannon G.A., Burks A., et al. Effects of cooking methods on peanut allergenicity. Journal of Allergy and Clinical Immunology 2001, 107:1077-1081.
7. Booth A.A., Khalifah R.G., Hudson B.G. Thiamine pyrophosphate and pyridoxamine inhibit the formation of antigenic advanced glycation end-products: comparison with aminoguanidine. Biochemical and Biophysical Research Communications 1996, 220:113-119.
8. Bouhallab S., Morgan F., Henry G., Mollé D., Léonil J. Formation of stable covalent dimer explains the high solubility at pH 4.6 of lactose-α-lactoglobulin conjugates heated near neutral pH. Journal of Agricultural and Food Chemistry 1999, 47:1489-1494.
9. Bu G., Lu J., Zheng Z., Luo Y. Influence of Maillard reaction conditions on the antigenicity of bovine α-lactalbumin using response surface methodology. Journal of the Science of Food and Agriculture 2009, 89:2428-2434.
10. Chicón R., Belloque J., Alonso E., López-Fandiño R. Immunoreactivity and digestibility of high-pressure-treated whey proteins. International Dairy Journal 2008, 18:367-376.
11. Chobert J.M., Briand L., Grinberg V., Haertlé T. Impact of esterification on the folding and the susceptibility to peptic proteolysis of β-lactoglobulin. Biochimica et Biophysica Acta 1995, 1248:170-176.
12. Corzo-Martínez M., Lebrón-Aguilar R., Villamiel M., Quintanilla-López J.E., Moreno F.J. Application of liquid chromatography-tandem mass spectrometry for the characterization of galactosylated and tagatosylated β-lactoglobulin peptides derived from in vitro gastrointestinal digestion. Journal of Chromatography A 2009, 1216:7205-7212.
13. Corzo-Martinez M., Moreno F.J., Olano A., Villamiel M. Structural characterization of bovine β-lactoglobulin-galactose/tagatose Maillard complexes by electrophoretic, chromatographic and spectroscopic methods. Journal of Agricultural and Food Chemistry 2008, 56:4244-4252.
14. Corzo-Martinez M., Moreno F.J., Olano A., Villamiel M. Role of pyridoxamine in the formation of the Amadori/Heyns compounds and aggregates during the glycation of β-lactoglobulin with galactose and tagatose. Journal of Agricultural and Food Chemistry 2010, 58:500-506.
15. Dalgalarrondo M., Dufour E., Chobert J.-M., Bertrand-Harb C., Haertlé T. Proteolysis of β-lactoglobulin and β-casein by pepsin in ethanolic media. International Dairy Journal 1995, 5:1-14.
16. Desrosiers T., Savoie L., Bergeron G., Parent G. Estimation of lysine damage in heated whey proteins by furosine determinations in conjunction with the digestion cell technique. Journal of Agricultural and Food Chemistry 1989, 37:1385-1391.
17. de Wit J.N. Nutritional and functional characteristics of whey proteins in food products. Journal of Dairy Science 1998, 81:597-608.
18. Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 1956, 28:350-356.
19. Ehn B.-M., Allmere T., Telemo E., Bengtsson U., Ekstrand B. Modification of IgE binding to β-lactoglobulin by fermentation and proteolysis of cow's milk. Journal of Agricultural and Food Chemistry 2005, 53:3743-3748.
20. Foegeding A.E., Davis J.P., Doucet D., McGuffey M.K. Advances in modifying and understanding whey protein functionality. Trends in Food Science and Technology 2002, 13:151-159.
21. Gruber P., Vieths S., Wangorsch A., Nerkamp J., Hofmann T. Maillard reaction and enzymatic browning affect the allergenicity of Pru av 1, the major allergen from cherry (Prunus avium). Journal of Agricultural and Food Chemistry 2004, 52:4002-4007.
22. Guo M.R., Fox P.F., Flynn A., Kindstedt P.S. Susceptibility of β-lactoglobulin and sodium caseinate to proteolysis by pepsin and trypsin. Journal of Dairy Science 1995, 78:2336-2344.
23. Hattori M., Miyakawa S., Ohama Y., Kawamura H., Yoshida T., To-o K., et al. Reduced immunogenicity of β-lactoglobulin by conjugation with acidic oligosaccharides. Journal of Agricultural and Food Chemistry 2004, 52:4546-4553.
24. Hattori M., Nagasawa K., Ametani A., Kaminogawa S., Takahashi K. Functional changes in β-lactoglobulin by conjugation with carboxymethyl dextran. Journal of Agricultural and Food Chemistry 1994, 42:2120-2125.
25. Hattori M., Nagasawa K., Ohgata K., Sone N., Fukuda A., Matsuda H., et al. Reduced immunogenicity of beta-lactoglobulin by conjugation with carboxymethyl dextran. Bioconjugate Chemistry 2000, 11:84-93.
26. Hattori M., Numamoto K., Kobayashi K., Takahashi K. Functional changes in β-lactoglobulin by conjugation with cationic saccharides. Journal of Agricultural and Food Chemistry 2000, 48:2050-2056.
27. Henle T., Klostermeyer H. The reactivity of the individual protein-bound lysine residues of α-casein a1 during the initial stages of the Maillard-reaction. International Dairy Federation special issue 9303. Protein and fat globule modifications by heat treatment, homogenization and other technological means for high quality dairy products 1993, (pp. 183-189), International Dairy Federation, Brussels, Belgium.
28. Iametti S., Rasmussen P., Frøkiær H., Ferranti P., Addeo F., Bonomi F. Proteolysis of bovine α-lactoglobulin during thermal treatment in subdenaturing conditions highlights some structural features of the temperature-modified protein and yields fragments with low immunoreactivity. European Journal of Biochemistry 2002, 269:1362-1372.
29. Jarvinen K.-M., Chatchatee P., Bardina L., Beyer K., Sampson H.A. IgE and IgG binding epitopes on α-lactalbumin and β-lactoglobulin in cow's milk allergy. International Archives in Allergy and Immunology 2001, 126:111-118.
30. Jimenez-Castaño L., Villamiel M., López-Fandiño R. Glycosylation of individual whey proteins by Maillard reaction using dextran of different molecular mass. Food Hydrocolloids 2007, 21:433-443.
31. Kato A. Industrial applications of Maillard-type protein polysaccharide conjugates. Food Science and Technology Research 2002, 8:193-199.
32. Kitabatake N., Kinekawa Y. Digestibility of bovine milk whey protein and β-lactoglobulin in vitro and in vivo. Journal of Agricultural and Food Chemistry 1998, 46:4917-4923.
33. Kobayashi K., Hirano A., Ohta A., Yoshida T., Takahashi K., Hattori M. Reduced immunogenicity of beta-lactoglobulin by conjugation with carboxymethyl dextran differing in molecular weight. Journal of Agricultural and Food Chemistry 2001, 49:823-831.
34. Lapolla A., Fedele D., Martano L., Arico N.C., Garbeglio M., Traldi P., et al. Advanced glycation end products: a highly complex set of biologically relevant compounds detected by mass spectrometry. Journal of Mass Spectrometry 2001, 36:370-378.
35. Lapolla A., Fedele D., Reitano R., Arico N.C., Seraglia R., Traldi P., et al. Enzymatic digestion and mass spectrometry in the study of advanced glycation end products/peptides. Journal of the American Society for Mass Spectrometry 2004, 15:496-509.
36. Lehrer S.B., Horner E., Reese G. Why are some proteins allergenic? Implications for biotechnology. CRC Critical Reviews in Food Science and Nutrition 1996, 36:553-564.
37. Mahe S., Messing B., Thuillier F., Tome D. Digestion of bovine milk proteins in patients with a high jejunostomy. American Journal of Clinical Nutrition 1991, 54:534-538.
38. Maleki S.J., Chung S., Champagne E.T., Raufman J.P. The effects of roasting on the allergenic properties of peanuts. Journal of Allergy and Clinical Immunology 2000, 106:763-768.
39. Mills E.N.C., Sancho A.I., Moreno J., Kostyra H. The effects of food processing on allergens. Managing allergens in food 2006, 117-133. Woodhead Publishing Ltd, Cambridge, United Kingdom. C. Mills, H. Wichers, H. Hoffmann-Sommergruber (Eds.).
40. Moreno F.J. Gastrointestinal digestion of food allergens: effect on their allergenicity. Biomedicine and Pharmacotherapy 2007, 61:50-60.
41. Moreno F.J., Jenkins J.A., Mellon F.A., Rigby N.M., Robertson J.A., Wellner N., et al. Mass spectrometry and structural characterization of 2S albumin isoforms from Brazil nuts (Bertholletia excelsa). Biochimica et Biophysica Acta - Proteins and Proteomics 2004, 1698:175-186.
42. Moreno F.J., Mackie A.R., Mills E.N.C. Phospholipid interactions protect the milk allergen alpha-lactalbumin from proteolysis during in vitro digestion. Journal of Agricultural and Food Chemistry 2005, 53:9810-9816.
43. 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 Journal 2005, 272:341-352.
44. Moreno F.J., Quintanilla-López J.E., Lebrón-Aguilar R., Olano A., Sanz M.L. Mass spectrometric characterization of glycated β-lactoglobulin peptides derived from galacto-oligosaccharides surviving the in vitro gastrointestinal digestion. Journal of the American Society for Mass Spectrometry 2008, 19:927-937.
45. Morgan F., Léonil J., Mollé D., Bouhallab S. Nonenzymatic lactosylation of bovine β-lactoglobulin under mild heat treatment leads to structural heterogeneity of the glycoforms. Biochemical and Biophysical Research Communications 1997, 236:413-417.
46. 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 behaviour and protein conformation. Journal of Agricultural and Food Chemistry 1999, 47:83-91.
47. Morgan F., Mollé D., Henry G., Vénien A., Léonil J., Peltre G., et al. Glycation of bovine β-lactoglobulin: effect on the protein structure. International Journal of Food Sciences and Technology 1999, 34:429-435.
48. Nakamura A., Sasaki F., Watanabe K., Ojiva T., Ahn D.-H., Saeki H. Changes in allergenicity and digestibility of squid tropomyosin during the Maillard reaction with ribose. Journal of Agricultural and Food Chemistry 2006, 54:9529-9534.
49. Nakamura A., Watanabe K., Ojima T., Ahn D.-H., Saeki H. Effect of Maillard reaction on allergenicity of scallop tropomyosin. Journal of Agricultural and Food Chemistry 2005, 53:7559-7564.
50. Nakamura S., Suzuki Y., Ishikawa E., Yakushi T., Jing H., Miyamoto T., et al. Reduction of in vitro allergenicity of buckwheat Fag e 1 through the Maillard-type glycosylation with polysaccharides. Food Chemistry 2008, 109:538-545.
51. Oliver C.M., Melton L.D., Stanley R.A. Creating proteins with novel functionality via the Maillard reaction: a review. Critical Reviews in Food Science and Nutrition 2006, 46:337-350.
52. Pastorello E.A., Pravettoni V., Calamari A.M., Banfi E., Robino A.M. New plant-origin food allergens. Allergy 2002, 57:106-110.
53. Peñas E., Préstamo G., Baeza M.L., Martínez-Molero M.I., Gómez R. Effect of enzymatic treatments on the hydrolysis and immunoreactivity of dairy whey proteins. International Dairy Journal 2006, 16:831-839.
54. 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. Journal of Agricultural and Food Chemistry 1988, 36:737-741.
55. Sanz M.L., Corzo-Martínez M., Rastall R.A., Olano A., Moreno F.J. Characterization and in vitro digestibility of bovine β-lactoglobulin glycated with galactooligosaccharides. Journal of Agricultural and Food Chemistry 2007, 55:7916-7925.
56. Sehon A.H. Suppression of IgE antibody responses with tolerogenic conjugates of allergens and haptens. Progress in Allergy 1982, 32:161-202.
57. Sélo I., Clément G., Bernard H., Chatel J.M., Crémion C., Peltre G., et al. Allergy to bovine β-lactoglobulin: specificity of human IgE to tryptic peptides. Clinical and Experimental Allergy 1999, 29:1055-1063.
58. Shin D.S., Compadre C.M., Maleki S.J., Kopper R.A., Sampson H., Huang S.K., et al. Journal of Biological Chemistry 1998, 273:13753-13759.
59. Simonato B., de Lazzari F., Pasini G., Polato F., Giannatasio M., Gemignani C., et al. IgE binding to soluble and insoluble wheat flour proteins in atopic and non-atopic patients suffering from gastrointestinal symptoms after wheat ingestion. Clinical and Experimental Allergy 2001, 31:1771-1778.
60. Stapelfeldt H., Petersen P.H., Kristiansen K.R., Qvist K.B., Skibsted L.H. Effect of high hydrostatic pressure on the enzymatic hydrolysis of α-lactoglobulin B by trypsin, thermolysin and pepsin. Journal of Dairy Research 1996, 63:111-118.
61. Taheri-Kafrani A., Gaudin J.-C., Rabesona H., Nioi C., Agarwal D., Drouet M., et al. Effects of heating and glycation of β-lactoglobulin on its recognition by IgE of sera from cow milk allergy patients. Journal of Agricultural and Food Chemistry 2009, 57:4974-4982.
62. Voziyan P.A., Metz T.O., Baynes J.W., Hudson B.G. A post-Amadori inhibitor pyridoxamine also inhibits chemical modification of proteins by scavenging carbonyl intermediates of carbohydrate and lipid degradation. Journal of Biological Chemistry 2002, 277:3397-3403.
63. Wal J.M. Structure and function of milk allergens. Allergy 2001, 56(Suppl. 67):35-38.
64. Yeboah F.K., Alli I., Yaylayan V.A., Yasuo K., Chowdhury S.F., Purisima E.O. Effect of limited solid-state glycation on the conformation of lysozyme by ESI-MSMS peptide mapping and molecular modeling. Bioconjugate Chemistry 2004, 15:27-34.