Insight into the Glycation of Milk Proteins: An ESI- and MALDI-MS Perspective (Review)

REFERENCES

• Abraham , E. C. , Huaqian , J. , Aziz , A. , Kumarasamy , A. and Datta , P. 2008 . Role of the specifically targeted lysine residues in the glycation dependent loss of chaperone activity of αA- and αB-crystallins. . Mol. Cell. Biochem. , 310 : 235 – 239 .
   PubMedGoogle Scholar
• Acharya , A. S. , Roy , R. P. and Dorai , B. 1991 . Aldimine to ketoamine isomerization (Amadori rearrangement) potential at the individual nonenzymic glycation sites of hemoglobin A: Preferential inhibition of glycation by nucleophiles at sites of low isomerization potential. . J. Protein Chem. , 10 : 345 – 358 .
   PubMedGoogle Scholar
• Aebersold , R. and Mann , M. 2003 . Mass spectrometry-based proteomics. . Nature , 422 : 198 – 207 .
   PubMed Web of Science ®Google Scholar
• Ahmed , N. , Mirshekar-Syahkal , B. , Kennish , L. , Karachalias , N. , Babael-Jadidi , R. and Thornalley , P. J. 2005 . Assay of advanced glycation endproducts in selected beverages and food by liquid chromatography with tandem mass spectrometric detection. . Mol. Nutr. Food Res. , 49 : 691 – 699 .
   PubMed Web of Science ®Google Scholar
• Alomirah , H. , Alli , I. and Konishi , Y. 2003 . Charge state distribution and hydrogen/deuterium exchange of α-lactalbumin and β-lactoglobulin preparations by electrospray ionization mass spectrometry. . J. Agric. Food Chem. , 51 : 2049 – 2057 .
   PubMedGoogle Scholar
• Ames , J. M. 2005 . Application of semiquantitative proteomics techniques to the Maillard reaction. . Ann. N.Y. Acad. Sci. , 1043 : 225 – 235 .
   PubMedGoogle Scholar
• Ames , J. M. 2008 . Mass spectrometry to detect the site specificity of advanced glycation/lipoxidation end-product formation on protein: Some challenges and solutions. . Biochem. Soc. Trans. , 36 : 1051 – 1054 .
   PubMedGoogle Scholar
• Arita , K. , Babiker , E. E. , Azakami , H. and Kato , A. 2001 . Effect of chemical and genetic attachment of polysaccharides to proteins on the production of IgG and IgE. . J. Agric. Food Chem. , 49 : 2030 – 2036 .
   PubMedGoogle Scholar
• Assar , S. H. , Moloney , C. , Lima , M. , Magee , R. and Ames , J. M. 2009 . Determination of N ϵ-(carboxymethyl)lysine in food systems by ultra performance liquid chromatography-mass spectrometry. . Amino Acids , 36 : 317 – 326 .
   PubMed Web of Science ®Google Scholar
• Babiker , E. E. , Hiroyuki , A. , Matsudomi , N. , Iwata , H. , Ogawa , T. , Bando , N. and Kato , A. 1998 . Effect of polysaccharide conjugation or transglutaminase treatment on the allergenicity and functional properties of soy protein. . J. Agric. Food Chem. , 46 : 866 – 871 .
   Web of Science ®Google Scholar
• Baynes , J. W. , Watkins , N. G. , Fisher , C. I. , Hull , C. J. , Patrick , J. S. , Ahmed , M. U. , Dunn , J. A. and Thorpe , S. R. 1989 . “ The Amadori product on protein ” . In The Maillard Reaction in Aging, Diabetes, and Nutrition , Edited by: Baynes , J.W. and Monnier , V. M. 43 – 67 . New York : Alan R. Liss .
   Google Scholar
• Berg , H. E. and van Boekel , M.A.J.S. 1994 . Degradation of lactose during heating of milk. 1. Reaction pathways. . Neth. Milk Dairy J. , 46 : 157 – 175 .
   Google Scholar
• van Boekel , M.A.J.S. 2001 . Kinetic aspects of the Maillard reaction: A critical review. . Nahrung , 45 : 150 – 159 .
   PubMedGoogle Scholar
• Bouhallab , S. , Morgan , F. , Henry , G. , Mollé , D. and Léonil , J. 1999 . Formation of stable covalent dimer explains the high solubility at pH 4.6 of lactose−β-lactoglobulin conjugates heated near neutral pH. . J. Agric. Food Chem. , 47 : 1489 – 1494 .
   PubMedGoogle Scholar
• Boye , J. I. and Alli , I. 2000 . Thermal denaturation of mixtures of α-lactalbumin and β-lactoglobulin: A differential scanning calorimetric study. . Food Res. Int. , 33 : 673 – 682 .
   Web of Science ®Google Scholar
• Boye , J. I. , Ma , C-Y. , Ismail , A. , Harwalkar , V. R. and Kalab , M. 1997 . Molecular and microstructural studies of thermal denaturation and gelation of β-lactoglobulins A and B. . J. Agric. Food Chem. , 45 : 1608 – 1618 .
   Web of Science ®Google Scholar
• Brock , J. W.C. , Hinton , D. J.S. , Cotham , W. E. , Metz , T. O. , Thorpe , S. R. , Baynes , J. W. and Ames , J. M. 2003 . Proteomic analysis of the site specificity of glycation and carboxymethylation of ribonuclease. . J. Proteome Res. , 2 : 506 – 513 .
   PubMedGoogle Scholar
• Broersen , K. , Voragen , A. G.J. , Hamer , R. J. and de Jongh , H.H.J. 2004 . Glycoforms of β-lactoglobulin with improved thermostability and preserved structural packing. . Biotech. Bioeng. , 86 : 78 – 87 .
   PubMedGoogle Scholar
• Broersen , K. , Elshof , M. , de Groot , J. , Voragen , A. G.J. , Hamer , R. J. and de Jongh , H.H.J. 2007 . Aggregation of β-lactoglobulin regulated by glucosylation. . J. Agric. Food Chem. , 55 : 2431 – 2437 .
   PubMed Web of Science ®Google Scholar
• Brown , E. M. , Pfeffer , P. E. , Kumosinski , T. F. and Greenberg , R. 1988 . Accessibility and mobility of lysine residues in β-lactoglobulin. . Biochem. , 27 : 5601 – 5610 .
   PubMedGoogle Scholar
• Brownlow , S. , Cabral , J. H.M. , Cooper , R. , Flower , D. R. , Yewdall , S. J. , Polikarpov , I. , North , A. C.T. and Sawyer , L. 1997 . Bovine β-lactoglobulin at 1.8Å resolution-still an enigmatic lipocalin. . Structure , 5 : 481 – 495 .
   PubMed Web of Science ®Google Scholar
• Burr , R. , Moore , C. H. and Hill , J. P. 1996 . Evidence of multiple glycosylation of bovine β-lactoglobulin by electrospray ionization mass spectrometry. . Milchwissenschaft , 51 : 488 – 492 .
   Google Scholar
• Capote , F. P. and Sanchez , J-C. 2009 . Strategies for proteomic analysis of non-enzymatically glycated proteins. . Mass Spectrom. Rev. , 28 : 135 – 146 .
   PubMedGoogle Scholar
• Chevalier , F. , Chobert , J-M. , Dalgalarrondo , M. and Haertlé , T. 2001a . Characterization of the Maillard reaction products of β-lactoglobulin glucosylated in mild conditions. . J. Food Biochem. , 25 : 33 – 55 .
   Web of Science ®Google Scholar
• Chevalier , F. , Chobert , J-M. , Mollé , D. and Haertlé , T. 2001b . Maillard glycation of β-lactoglobulin with several sugars: Comparative study of the properties of the obtained polymers and of the substituted sites. . Lait , 81 : 651 – 666 .
   Google Scholar
• Chevalier , F. , Hirtz , C. , Sommerer , N. and Kelly , A. L. 2009 . Use of reducing/nonreducing two-dimensional electrophoresis for the study of disulfide-mediated interactions between proteins in raw and heated bovine milk. . J. Agric. Food Chem. , 57 : 5948 – 5955 .
   PubMedGoogle Scholar
• Chung , S-Y. and Champagne , E. T. 1999 . Allergenicity of Maillard reaction products from peanut proteins. . J. Agric. Food Chem. , 47 : 5227 – 5231 .
   PubMed Web of Science ®Google Scholar
• Costantino , H. R. , Langer , R. and Klibanov , A. M. 1994 . Solid-phase aggregation of proteins under pharmaceutically relevant conditions. . J. Pharm. Sci. , 83 : 1662 – 1669 .
   PubMed Web of Science ®Google Scholar
• Corzo-Martínez , M. , Moreno , F. J. , Olano , A. and Villamiel , M. 2008 . Structural characterization of bovine β-lactoglobulin−galactose/tagatose Maillard complexes by electrophoretic, chromatographic, and spectroscopic methods. . J. Agric. Food Chem. , 56 : 4244 – 4252 .
   PubMed Web of Science ®Google Scholar
• Corzo-Martínez , M. , Moreno , F. J. , Villamiel , M. and Harte , F. M. 2010 . Characterization and improvement of rheological properties of sodium caseinate glycated with galactose, lactose and dextran. . Food Hydrocolloids , 24 ( 1 ) : 88 – 97 .
   Web of Science ®Google Scholar
• Cotham , W. E. , Hinton , D. J.S. , Metz , T. O. , Brock , J. W.C. , Thorpe , S. R. , Baynes , J. W. and Ames , J. M. 2003 . Mass spectrometric analysis of glucose-modified ribonuclease. . Biochem. Soc. Trans. , 31 : 1426 – 1427 .
   PubMedGoogle Scholar
• Czerwenka , C. , Maier , I. , Pittner , F. and Lindner , W. 2006 . Investigation of the lactosylation of whey proteins by liquid chromatography-mass spectrometry. . J. Agric. Food Chem. , 54 : 8874 – 8888 .
   PubMed Web of Science ®Google Scholar
• Dai , Z. , Wang , B. , Sun , G. , Fan , X. , Anderson , V. and Monnier , V. M. 2008 . Identification of glucose-derived cross-linking sites in ribonuclease A. . J. Proteome Res. , 7 : 2756 – 2768 .
   PubMed Web of Science ®Google Scholar
• Dalgalarrondo , M. , Chobert , J-M. , Dufour , E. , Bertrand-Harb , C. , Dumont , J-P. and Haertlé , T. 1990 . Influence of pH on the structural changes of β-lactoglobulin studied by tryptic hydrolysis. . Biochim. Biophys. Acta , 1077 : 31 – 34 .
   Google Scholar
• Dalgleish , D. G. , Senaratne , V. and Francois , S. 1997 . Interactions between α-lactalbumin and β-lactoglobulin in the early stages of heat denaturation. . J. Agric. Food Chem. , 45 : 3459 – 3464 .
   Web of Science ®Google Scholar
• Dalsgaard , T. K. , Nielsen , J. H. and Larsen , L. B. 2007 . Proteolysis of milk proteins lactosylated in model systems. . Mol. Nutr. Food Res. , 51 : 404 – 414 .
   PubMedGoogle Scholar
• Damodaran , S. 1996 . “ Amino acids, peptides, and proteins ” . In Food Chemistry , Edited by: Fennema , O. 321 – 430 . New York : Marcel Dekker .
   Google Scholar
• Darewicz , M. and Dziuba , J. 2001 . The effect of glycosylation on emulsifying and structural properties of bovine β-casein. . Nahrung , 45 : 15 – 20 .
   PubMedGoogle Scholar
• de Jongh , H.H.J. , Gröneveld , T. and de Groot , J. 2001 . Mild isolation procedure discloses new protein structural properties of β-lactoglobulin. . J. Dairy Sci. , 84 : 562 – 571 .
   PubMed Web of Science ®Google Scholar
• Delatour , T. , Hegele , J. , Parisod , V. , Richoz , J. , Maurer , S. , Steven , M. and Buetler , T. 2009 . Analysis of advanced glycation endproducts in dairy products by isotope dilution liquid chromatography-electrospray tandem mass spectrometry. The particular case of carboxymethyllysine. . J. Chromatogr. A , 1216 : 2371 – 2381 .
   PubMed Web of Science ®Google Scholar
• Dong , A. , Matsuura , J. , Allison , S. D. , Chrisman , E. , Manning , M. C. and Carpenter , J. F. 1996 . Infrared and circular dichroism spectroscopic characterization of structural differences between β-lactoglobulin A and B. . Biochem. , 35 : 1450 – 1457 .
   PubMed Web of Science ®Google Scholar
• Donato , L. and Guyomarc'h , F. 2009 . Formation and properties of the whey protein/κ-casein complexes in heated skim milk: A review. . Dairy Sci. Technol. , 89 : 3 – 29 .
   Web of Science ®Google Scholar
• Farah , M. A. , Bose , S. , Lee , J-H. , Jung , H-C. and Kim , Y. 2005 . Analysis of glycated insulin by MALDI-TOF mass spectrometry. . Biochim. Biophys. Acta , 1725 : 269 – 282 .
   PubMed Web of Science ®Google Scholar
• Farrell , H. M. , Jimenez-Flores , R. , Bleck , G. T. , Brown , E. M. , Butler , J. E. , Creamer , L. K. , Hicks , C. L. , Hollar , C. M. , Ng-Kwai-Hang , K.F. and Swaisgood , H. E. 2004 . Nomenclature of the proteins of cows' milk. (Sixth revision) . J. Dairy Sci. , 87 : 1641 – 1674 .
   PubMed Web of Science ®Google Scholar
• Fay , L. B. and Brevard , H. 2005 . Contribution of mass spectrometry to the study of the Maillard reaction in food. . Mass Spectrom. Rev. , 24 : 487 – 507 .
   PubMed Web of Science ®Google Scholar
• Fenaille , F. , Campos-Giménez , E. , Guy , P. A. , Schmitt , C. and Morgan , F. 2003a . Monitoring of β-lactoglobulin dry-state glycation using various analytical techniques. . Anal. Biochem. , 320 : 144 – 148 .
   PubMed Web of Science ®Google Scholar
• Fenaille , F. , Morgan , F. , Parisod , V. , Tabet , J-C. and Guy , P. A. 2003b . Solid-state glycation of β-lactoglobulin monitored by electrospray ionisation mass spectrometry and gel electrophoresis techniques. . Rapid Commun. Mass Spectrom. , 17 : 1483 – 1492 .
   PubMedGoogle Scholar
• Fenaille , F. , Morgan , F. , Parisod , V. , Tabet , J-L. and Guy , P. 2004 . Solid-state glycation of β-lactoglobulin by lactose and galactose: Localization of the modified amino acids using mass spectrometric techniques. . J. Mass Spectrom. , 39 : 16 – 28 .
   PubMed Web of Science ®Google Scholar
• Fenaille , F. , Parisod , V. , Tabet , J-C. and Guy , P. A. 2005 . Carbonylation of milk powder proteins as a consequence of processing conditions. . Proteomics , 5 : 3097 – 3104 .
   PubMed Web of Science ®Google Scholar
• Fenaille , F. , Parisod , V. , Visani , P. , Populaire , S. , Tabet , J-C. and Guy , P. A. 2006 . Modifications of milk constituents during processing: A preliminary benchmarking study. . Int. Dairy J. , 16 : 728 – 739 .
   Web of Science ®Google Scholar
• Fenn , J. B. , Mann , M. , Meng , C. K. , Wong , S. F. and Whitehouse , C. M. 1989 . Electrospray ionization of mass spectrometry of large biomolecules. . Sci. , 246 : 64 – 71 .
   PubMed Web of Science ®Google Scholar
• Fogliano , V. , Monti , S. M. , Visconti , A. , Randazzo , G. , Facchiano , A. M. , Colonna , G. and Ritieni , A. 1998 . Identification of β-lactoglobulin lactosylation site. . Biochim. Biophys. Acta , 1388 : 295 – 304 .
   PubMedGoogle Scholar
• Fogolari , F. , Ragona , L. , Licciardi , S. , Romagnoli , S. , Michelutti , R. , Ugolini , R. and Molinari , H. 2000 . Electrostatic properties of bovine β-lactoglobulin. . Proteins Struct. Funct. Genet. , 39 : 317 – 330 .
   PubMedGoogle Scholar
• Foltz , M. , Ansems , P. , Schwarz , J. , Tasker , M. C. , Lourbakos , A. and Gerhardt , C. C. 2008 . Protein hydrolysates induce CCK release from enteroendocrine cells and act as partial agonists of the CCK1 receptor. . J. Agric. Food Chem. , 56 : 837 – 843 .
   PubMed Web of Science ®Google Scholar
• Fox , P. F. 1997 . Advanced Dairy Chemistry. Vols. 1–3 Elsevier, NY
   Google Scholar
• French , S. J. and Harper , W. J. 2001 . Theoretical representation of surface properties on hypothetical Maillard modified β-lactoglobulin using GRASP/GRASS. . Milchwissenschaft , 56 : 310 – 313 .
   Google Scholar
• French , S. J. and Harper , W. J. 2003 . Maillard reaction induced lactose attachment to bovine β-lactoglobulin: Foam and emulsion functionality. . Milchwissenschaft , 58 : 252 – 255 .
   Google Scholar
• French , S. J. , Harper , W. J. , Kleinholz , N. M. , Jones , R. B. and Green-Church , K.B. 2002 . Maillard reaction induced lactose attachment to bovine β-lactoglobulin: Electrospray ionization and matrix-assisted laser desorption/ionization examination. . J. Agric. Food Chem. , 50 : 820 – 823 .
   PubMedGoogle Scholar
• Gadgil , H. S. , Bondarenko , P. V. , Treuheit , M. J. and Ren , D. 2007 . Screening and sequencing of glycated proteins by neutral loss scan LS/MS/MS method. . Anal. Chem. , 79 : 5991 – 5999 .
   PubMed Web of Science ®Google Scholar
• Galani , D. and Apenten , R. K.O. 1997 . The comparative heat stability of bovine β-lactoglobulin in buffer and complex media. . J. Sci. Food Agric. , 74 : 89 – 98 .
   Google Scholar
• Galvani , M. , Hamdan , M. and Righetti , P. G. 2000 . Two-dimensional gel electrophoresis/matrix-assisted laser desorption/ionisation mass spectrometry of a milk powder. . Rapid Commun. Mass Spectrom. , 14 : 1889 – 1897 .
   PubMedGoogle Scholar
• Gauthier , F. , Bouhallab , S. and Renault , A . 2001 . Modification of bovine β-lactoglobulin by glycation in a powdered state or in aqueous solution: Adsorption at the air-water interface. . Colloids Surf. B. , 21 : 37 – 45 .
   PubMed Web of Science ®Google Scholar
• Gough , P. and Jenness , R. 1962 . Heat denaturation of β-lactoglobulins A and B. . J. Dairy Sci. , 45 : 1033 – 1039 .
   Web of Science ®Google Scholar
• Grandori , R. 2003 . Electrospray-ionization mass spectrometry for protein conformational studies. . Curr. Org. Chem. , 7 : 1589 – 1603 .
   Google Scholar
• Guedes , S. , Vitorino , R. , Domingues , M. R.M. , Amado , F. and Domingues , P. 2009 . Mass spectrometry characterization of the glycation sites of bovine insulin by tandem mass spectrometry. . J. Am. Soc. Mass Spectrom. , 20 : 1319 – 1326 .
   PubMedGoogle Scholar
• Guy , P. A. and Fenaille , F. 2006 . Contribution of mass spectrometry to assess quality of milk-based products. . Mass Spectrom. Reviews , 25 : 290 – 326 .
   PubMed Web of Science ®Google Scholar
• Guyomarc'h , F. , Warin , F. , Muir , D. and Leaver , J. 2000 . Lactosylation of milk powders during the manufacture and storage of skim milk powders. . Int. Dairy J. , 10 : 863 – 872 .
   Web of Science ®Google Scholar
• Hageman , M. J. 1992 . “ Water sorption and solid-state stability of proteins ” . In Stability of Protein Pharmaceuticals. Part A: Chemical and Physical Pathways of Protein Degradation , Edited by: Ahern , T.J. and Manning , M. C. 273 – 309 . New York : Plenum Press .
   Google Scholar
• Hattori , M. , Miyakawa , S. , Ohama , Y. , Kawamura , H. , Yoshida , T. , To-o , K. , Kuriki , T. and Takahashi , K. 2004 . Reduced immunogenicity of β-lactoglobulin by conjugation with acidic oligosaccharides. . J. Agric. Food Chem. , 52 : 4546 – 4553 .
   PubMed Web of Science ®Google Scholar
• Hau , J. and Bovetto , L. 2001 . Characterisation of modified whey protein in milk ingredients by liquid chromatography coupled to electrospray ionisation mass spectrometry. . J. Chromatogr. A , 926 : 105 – 112 .
   PubMed Web of Science ®Google Scholar
• Hegele , J. , Buetler , T. and Delatour , T. 2008a . Comparative LC-MS/MS profiling of free and protein-bound early and advanced glycation-induced lysine modifications in dairy products. . Anal. Chim. Acta , 617 : 8 – 96 .
   Google Scholar
• Hegele , J. , Parisod , V. , Richoz , J. , Förster , A. , Maurer , S. , Krause , R. , Henle , T. , Bütler , T. and Delatour , T. 2008b . Evaluating the extent of protein damage in dairy products. Simultaneous determination of early and advanced glycation-induced lysine modifications. . Ann. N.Y. Acad. Sci. , 1126 : 300 – 306 .
   PubMedGoogle Scholar
• Henle , T. and Klostermeyer , H. 1993 . “ The reactivity of the individual protein-bound lysine residues of β-casein A during the initial stages of the Maillard reaction ” . In Protein and Fat Globule Modifications by Heat Treatment, Homogenization & other Technological means for High Quality Dairy Products 183 – 189 . IDF Special Issue 9303, Brussels, IDF.
   Google Scholar
• Hillier , R. M. , Lyster , R. L.J. and Cheeseman , G. C. 1979 . Thermal denaturation of α-la and β-lg in cheese whey: Effect of total solids concentration and pH. . J. Dairy Res. , 46 : 103 – 111 .
   Web of Science ®Google Scholar
• Hinton , D. J.S. and Ames , J. M. 2006 . Site specificity of glycation and carboxymethylation of bovine serum albumin by fructose. . Amino Acids , 30 : 425 – 433 .
   PubMed Web of Science ®Google Scholar
• Hodge , J. E. 1953 . Dehydrated foods. Chemistry of browning reactions in model systems. . Agric. food Chem. , 1 : 928 – 943 .
   Web of Science ®Google Scholar
• Hop , C.E.C.A. and Bakhtiar , R. 1997 . An introduction to electrospray ionization and matrix-assisted laser desorption/ionization mass spectrometry: Essential tools in a modern biotechnology environment. . Biospectroscopy , 3 : 259 – 280 .
   Google Scholar
• Huang , X. L. , Catignani , G. L. and Swaisgood , H. E. 1994 . Relative structural stabilities of β-lactoglobulins A and B as determined by proteolytic susceptibility and differential scanning calorimetry. . J. Agric. Food Chem. , 42 : 1276 – 1280 .
   Google Scholar
• Humeny , A. , Kislinger , T. , Becker , C-M. and Pischetsrieder , M. 2002 . Qualitative determination of specific protein glycation products by matrix-assisted laser desorption/ionization mass spectrometry peptide mapping. . J. Agric. Food Chem. , 50 : 2153 – 2160 .
   PubMedGoogle Scholar
• Jones , A. D. , Tier , C. M. and Wilkins , J. P.G. 1998 . Analysis of Maillard reaction products of β-lactoglobulin and lactose in skimmed milk powder by capillary electrophoresis and electrospray mass spectrometry. . J. Chromatogr. A , 822 : 147 – 154 .
   PubMed Web of Science ®Google Scholar
• Jost , R. 1993 . Functional characteristics of dairy proteins. . Trends Food Sci. Technol. , 4 : 283 – 288 .
   Google Scholar
• Karas , M. and Hillenkamp , F. 1988 . Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. . Anal. Chem. , 60 : 2299 – 2301 .
   PubMed Web of Science ®Google Scholar
• Kinsella , J. E. 1984 . Milk proteins: Physicochemical and functional properties. . Crit. Rev. Food Sci. Nutr. , 21 : 197 – 262 .
   PubMed Web of Science ®Google Scholar
• Kislinger , T. , Humeny , A. , Peich , C. C. , Becker , C-M. and Pischetsrieder , M. 2005 . Analysis of protein glycation products by MALDI-TOF/MS. . Ann. N.Y. Acad. Sci. , 1043 : 249 – 259 .
   PubMed Web of Science ®Google Scholar
• Kislinger , T. , Humeny , A. , Peich , C. C. , Zhang , X. , Niwa , T. , Pischetsrieder , M. and Becker , C-M. 2003 . Relative quantification of N-(carboxymethyl)lysine, imidazolone A and the Amadori product in glycated lysozyme by MALDI-TOF mass spectrometry. . J. Agric. Food Chem. , 51 : 51 – 57 .
   PubMedGoogle Scholar
• Kislinger , T. , Humeny , A. and Pischetsrieder , M. 2004 . Analysis of protein glycation products by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. . Curr. Med. Chem. , 11 : 2185 – 2193 .
   PubMedGoogle Scholar
• Kroh , L. W. and Schulz , A. 2001 . News on the Maillard reaction of oligomeric carbohydrates: A survey. . Nahrung , 45 : 160 – 163 .
   PubMedGoogle Scholar
• Kumar , P. A. , Kumar , M. S. and Reddy , G. B. 2007 . Effect of glycation on α-crystallin structure and chaperone-like function. . Biochem. J. , 408 : 251 – 258 .
   PubMed Web of Science ®Google Scholar
• Labuza , T. P. and Baisier , W. M. 1992 . “ The kinetics of nonenzymatic browning ” . In Physical Chemistry of Foods , Edited by: Schwartberg , H.G. and Hartel , R. W. 595 – 649 . New York : Marcel Dekker .
   Google Scholar
• Lapolla , A. , Fedele , D. , Reitano , R. , Aricò , N. C. , Seraglia , R. , Traldi , P. , Marotta , E. and Tonani , R. 2004 . Enzymatic digestion and mass spectrometry in the study of advanced glycation end products/peptides. . J. Am. Soc. Mass Spectrom. , 15 : 496 – 509 .
   PubMed Web of Science ®Google Scholar
• Lapolla , A. , Brancia , F. L. , Bereszczak , J. , Fedele , D. , Baccarin , L. , Seraglia , R. and Traldi , P. 2007 . Off-line liquid chromatography-MALDI by with various matrices and tandem mass spectrometry for analysis of glycated serum albumin tryptic peptides. . Mol. Nutr. Food Res. , 51 : 456 – 461 .
   PubMedGoogle Scholar
• Ledesma-Osuna , A. I. , Ramos-Clamont , G. and Vázquez-Moreno , L. 2008 . Characterization of bovine serum albumin glycated with glucose, galactose and lactose. . Acta Biochim. Polonica , 55 : 491 – 497 .
   PubMed Web of Science ®Google Scholar
• Léonil , J. , Gagnaire , V. , Mollé , D. , Pezennec , S. and Bouhallab , S. 2000 . Application of chromatography and mass spectrometry to the characterization of food proteins and peptides. . J. Chromatogr. A , 881 : 1 – 21 .
   PubMed Web of Science ®Google Scholar
• Léonil , J. , Mollé , D. , Fauquant , J. , Maubois , J. L. , Pearce , R. J. and Bouhallab , S. 1997 . 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. , 80 : 2270 – 2281 .
   PubMed Web of Science ®Google Scholar
• Lillard , J. S. , Clare , D. A. and Daubert , C. R. 2009 . Glycosylation and expanded utility of a modified whey protein ingredient via carbohydrate conjugation at low pH. . J. Dairy Sci. , 92 : 35 – 48 .
   PubMed Web of Science ®Google Scholar
• Lima , M. , Moloney , C. and Ames , J. M. 2009 . Ultra performance liquid chromatography-mass spectrometric determination of the site specificity of modification of β-casein by glucose and methylglyoxal. . Amino Acids , 36 : 475 – 481 .
   PubMedGoogle Scholar
• Losito , I. , Carbonara , T. , Monaci , L. and Palmisano , F. 2007 . Evaluation of the thermal history of bovine milk from the lactosylation of whey proteins: An investigation by liquid chromatography–electrospray ionization mass spectrometry. . Ann. Bioanal. Chem. , 389 : 2065 – 2074 .
   PubMedGoogle Scholar
• Lund , M. N. , Olsen , K. , Sørensen , J. and Skibsted , L. H. 2005 . Kinetics and mechanism of lactosylation of α-lactalbumin. . J. Agric. Food Chem. , 53 : 2095 – 2102 .
   PubMed Web of Science ®Google Scholar
• Madureira , A. R. , Pereira , C. I. , Gomes , A. M.P. , Pintado , M. E. and Malcata , F. X. 2007 . Bovine whey proteins: Overview on their main biological properties. . Food Res. Int. , 40 : 1197 – 1211 .
   Web of Science ®Google Scholar
• Maillard , L-C. 1912 . Action des acides amines sur les sucres. Formation des melanoidins par voie methodiqué . Compt. Rend. Hebd. Seances Acad. Sci. , 154 : 66 – 68 .
   Google Scholar
• Marvin , L. F. , Parisod , V. , Fay , L. B. and Guy , P. A. 2002 . Characterization of lactosylated proteins of infant formula powders using two-dimensional gel electrophoresis and nanoelectrospray mass spectrometry. . Electrophoresis , 23 : 2505 – 2512 .
   PubMed Web of Science ®Google Scholar
• Mann , M. , Hendrickson , R. C. and Pandey , A. 2001 . Analysis of proteins and proteomes by mass spectrometry. . Annu. Rev. Biochem. , 70 : 437 – 473 .
   PubMed Web of Science ®Google Scholar
• Mauron , J. 1990 . Influence of processing on protein quality. . J. Nutr. Sci. Vitaminol. , 36 : 557 – 569 .
   Google Scholar
• McSweeney , P. H.L. and Fox , P. F. 2009 . Advanced Dairy Chemistry:.Lactose, Water, Salts and Minor Constituents, Vol. 3 , New York : Springer-Verlag .
   Google Scholar
• Medrano , A. , Abirached , C. , Panizzolo , L. , Moyna , P. and Añón , M. C. 2009 . The effect of glycation on foam and structural properties of β-lactoglobulin. . Food Chem. , 113 : 127 – 133 .
   Web of Science ®Google Scholar
• Meltretter , J. and Pischetsrieder , M. 2008 . Application of mass spectrometry for the detection of glycation and oxidation products in milk proteins. . Ann. N.Y. Acad. Sci. , 1126 : 134 – 140 .
   PubMed Web of Science ®Google Scholar
• Meltretter , J. , Becker , C-M. and Pischetsrieder , M. 2008a . Identification and site-specific relative quantification of β-lactoglobulin modifications in heated milk and dairy products. . J. Agric. Food Chem. , 56 : 5165 – 5171 .
   PubMed Web of Science ®Google Scholar
• Meltretter , J. , Birlouez-Aragon , I. , Becker , C-M. and Pischetsrieder , M. 2009 . Assessment of heat treatment of dairy products by MALDI-TOF-MS. . Mol. Nutr. Food Res. , 53 : 1 – 9 .
   Google Scholar
• Meltretter , J. , Schmidt , A. , Humeny , A. , Becker , C-M. and Pischetsrieder , M. 2008b . Analysis of the peptide profile of milk and its changes during thermal treatment and storage. . J. Agric. Food Chem. , 56 : 2899 – 2906 .
   PubMed Web of Science ®Google Scholar
• Meltretter , J. , Seeber , S. , Humeny , A. , Becker , C-M. and Pischetsrieder , M. 2007 . Site-specific formation of Maillard, oxidation, and condensation products from whey proteins during reaction with lactose. . J. Agric. Food Chem. , 55 : 6096 – 6103 .
   PubMed Web of Science ®Google Scholar
• Mollé , D. , Morgan , F. , Bouhallab , S. and Léonil , J. 1998 . Selective detection of lactolated peptides in hydrosylates by liquid chromatography/electrospray tandem mass spectrometry. . Anal. Biochem. , 259 : 152 – 161 .
   PubMedGoogle Scholar
• Monaci , L. and van Hengel , A.J. 2007 . Effect of heat treatment on the detection of intact bovine β-lactoglobulins by LC mass spectrometry. . J. Agric. Food Chem. , 55 : 2985 – 2992 .
   PubMedGoogle Scholar
• Monaci , L. , Tregoat , V. , van Hengel , A.J. and Anklam , E. 2006 . Milk allergens, their characteristics and their detection in food: A review. . Eur. Food Res. Technol. , 223 : 149 – 179 .
   Web of Science ®Google Scholar
• Moreno , F. J. , López-Fandiño , R. and Olano , A. 2002 . Characterization and functional properties of lactosyl caseinomacropeptide conjugates. . J. Agric. Food Chem. , 50 : 5179 – 5184 .
   PubMedGoogle Scholar
• Moreno , F. J. , Quintanilla-López , J.E. , Lebrón-Aguilar , R. , Olano , A. and Sanz , M. L. 2008 . Mass spectrometric characterization of glycated β-lactoglobulin peptides derived from galacto-oligosaccharides surviving the in vitro gastrointestinal digestion. . J. Am. Soc. Mass Spectrom. , 19 : 927 – 937 .
   PubMed Web of Science ®Google Scholar
• Morgan , F. , Léonil , J. , Mollé , D. and Bouhallab , S. 1997 . Nonenzymatic lactosylation of bovine β-lactoglobulin under mild heat treatment leads to structural heterogeneity of the glycoforms. . Biochem. Biophys. Res. Commun. , 236 : 413 – 417 .
   PubMed Web of Science ®Google Scholar
• Morgan , F. , Bouhallab , S. , Mollé , D. , Henry , G. , Maubois , J-L. and Léonil , J. 1998 . Lactolation of β-lactoglobulin monitored by electrospray ionization mass spectrometry. . Int. Dairy J. , 8 : 95 – 98 .
   Web of Science ®Google Scholar
• Morgan , F. , Léonil , J. , Mollé , D. and Bouhallab , S. 1999a . 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. , 47 : 83 – 91 .
   PubMed Web of Science ®Google Scholar
• Morgan , F. , Mollé , D. , Henry , G. , Vénien , A. , Léonil , J. , Peltre , G. , Levieux , D. , Maubois , J-L. and Bouhallab , S. 1999b . Glycation of bovine β-lactoglobulin: Effect on the protein structure. . Int. J. Food Sci.Technol. , 34 : 429 – 435 .
   Web of Science ®Google Scholar
• Morgan , F. , Vénien , A. , Bouhallab , S. , Mollé , D. , Léonil , J. , Peltre , G. and Levieux , D. 1999c . Modification of bovine β-lactoglobulin by glycation in a powdered state or in an aqueous solution: Immunochemical characterization. . J. Agric. Food Chem. , 47 : 4543 – 4548 .
   PubMedGoogle Scholar
• Mouécoucou , J. , Frémont , S. , Villaume , C. , Sanchez , C. and Méjean , L. 2007 . Polysaccharides reduce in vitro IgG/IgE-binding of β-lactoglobulin after hydrolysis. . Food Chem. , 104 : 1242 – 1249 .
   Google Scholar
• Muslow , B. B. , Jacob , M. and Henle , T. 2009 . Studies on the impact of glycation on the denaturation of whey proteins. . Eur. Food Res. Technol. , 228 : 643 – 649 .
   Google Scholar
• Nacharaju , P. and Acharya , A. S. 1992 . Amadori rearrangement potential of hemoglobin at its glycation sites is dependent on the three-dimensional structure of protein. . Biochem. , 31 : 12673 – 12679 .
   PubMed Web of Science ®Google Scholar
• Nacka , F. , Chobert , J-M. , Burova , T. , Léonil , J. and Haertlé , T. 1998 . Induction of new physicochemical and functional properties by the glycosylation of whey proteins. . J. Protein Chem. , 17 : 495 – 503 .
   PubMedGoogle Scholar
• Nagaraj , R. H. , Biswas , A. , Miller , A. , Ova-ito , T. and Bhat , M. 2008 . The other side of the Maillard reaction. . Ann. N.Y. Acad. Sci. , 1126 : 107 – 112 .
   PubMedGoogle Scholar
• Natale , M. , Bisson , C. , Monti , G. , Peltran , A. , Garoffo , L. P. , Valentini , S. , Fabris , C. , Bertino , E. , Coscia , A. and Conti , A. 2004 . Cow's milk allergens identification by two-dimensional immunoblotting and mass spectrometry. . Mol. Nutr. Food Res. , 48 : 363 – 369 .
   PubMed Web of Science ®Google Scholar
• O'Donnell , R. , Holland , J. W. , Deeth , H. C. and Alewood , P. 2004 . Milk proteomics. . Int. Dairy J. , 14 : 1013 – 1023 .
   Web of Science ®Google Scholar
• Oliver , C. M. , Melton , L. D. and Stanley , R. A. 2003 . Sugar-protein conjugates and their formation WO03045163
   Google Scholar
• Oliver , C. M. , Stanley , R. A. and Melton , L. D. 2006 . Creating proteins with novel functionality through the Maillard reaction. . Crit. Rev. Food Sci. Nutr. , 46 : 337 – 350 .
   PubMed Web of Science ®Google Scholar
• Pan , G. G. , Oliver , C. M. and Melton , L. D. 2006 . α-Dicarbonyl compounds formed by nonenzymatic browning during the dry heating of caseinate and lactose. . J. Agric. Food Chem. , 54 : 6852 – 6857 .
   PubMedGoogle Scholar
• Prabakaran , S. and Damadoran , S . 1997 . Thermal unfolding of β-lactoglobulin: Characterization of initial unfolding events responsible for heat-induced aggregation. . J. Agric. Food Chem. , 45 : 4303 – 4308 .
   Google Scholar
• Sakurai , K. and Goto , Y. 2007 . Principal component analysis of the pH-dependent conformational transitions of bovine beta-lactoglobulin monitored by heteronuclear NMR. . PNAS , 104 : 15346 – 15351 .
   PubMedGoogle Scholar
• Sanz , M. L. , Corzo-Martínez , M. , Rastall , R. A. , Olano , A. and Moreno , F. J. 2007 . Characterization and in vitro digestibility of bovine β-lactoglobulin glycated with galactooligosaccharides. . J. Agric. Food Chem. , 55 : 7916 – 7925 .
   PubMed Web of Science ®Google Scholar
• Sawyer , L. , Kontopidis , G. and Wu , S-Y. 1999 . β-lactoglobulin –a three-dimenional perspective. . Int. J. Food Sci. Technol. , 34 : 409 – 418 .
   Google Scholar
• Scaloni , A. , Perillo , V. , Franco , P. , Fedele , E. , Froio , R. , Ferrara , L. and Bergamo , P. 2002 . Characterization of heat-induced lactosylation products in caseins by immunoenzymatic and mass spectrometric techniques. . Biochim. Biophys. Acta , 1598 : 30 – 39 .
   PubMedGoogle Scholar
• Siciliano , R. , Rega , B. , Amoresano , A. and Pucci , P. 2000 . Modern mass spectrometric methodologies in monitoring milk quality. . Anal. Chem. , 72 : 408 – 415 .
   PubMedGoogle Scholar
• Steffan , W. , Balzer , H. H. , Lippert , F. , Sambor , B. C. , Bradbury , A. G.W. and Henlé , T. 2006 . Characterization of casein lactosylation by capillary electrophoresis and mass spectrometry. . Eur. Food Res. Technol. , 222 : 467 – 471 .
   Google Scholar
• Sun , Y. , Hayakawa , S. , Ogawa , M. and Izumori , K. 2005 . Evaluation of the site specific protein glycation and antioxidant capacity of rare sugar-protein/peptide conjugates. . J. Agric. Food Chem. , 53 : 10205 – 10212 .
   PubMedGoogle Scholar
• Tagami , U. , Akashi , S. , Mizukoshi , T. , Suzuki , E. and Hirayama , K. 2000 . Structural studies of the Maillard reaction products of a protein using ion trap mass spectrometry. . J. Mass Spectrom. , 35 : 131 – 138 .
   PubMedGoogle Scholar
• Tsuda , H. , Sekine , K. , Ushida , Y. , Kuhara , T. , Takasuka , N. , Iigo , M. , Han , B. S. and Moore , M. A. 2000 . Milk and dairy products in cancer prevention: Focus on bovine lactoferrin. . Mutat. Res. , 462 : 227 – 233 .
   PubMed Web of Science ®Google Scholar
• Van Teeffelen , A.M.M. , Boersen , K. and de Jongh , H.H.J. 2005 . Glucosylation of β-lactoglobulin lowers the heat capacity change of unfolding: A unique way to affect protein thermodynamics. . Protein Sci. , 14 : 2187 – 2194 .
   PubMed Web of Science ®Google Scholar
• Wa , C. , Cemy , R. L. , Clarke , W. A. and Hage , D. S. 2007 . Characterization of glycation adducts on human serum albumin by matrix-assisted laser desorption/ionization time-of–flight mass spectrometry. . Clin. Chim. Acta , 385 : 48 – 60 .
   PubMed Web of Science ®Google Scholar
• Wal , J-M. 2003 . Thermal processing and allergenicity of foods. . Allergy , 58 : 727 – 729 .
   PubMed Web of Science ®Google Scholar
• Walstra , P. and Jenness , R. 1984 . Dairy Chemistry and Physics , New York : John Wiley and Sons .
   Google Scholar
• Walton , D. J. and Shilton , B. H. 1991 . Site specificity of protein glycation. . Amino Acids , 1 : 199 – 203 .
   PubMedGoogle Scholar
• Wu , S-Y. , Pérez , M. D. , Puyol , P. and Sawyer , L. 1999 . β-Lactoglobulin binds palmitate within its central cavity. . J. Biol. Chem. , 274 : 170 – 174 .
   PubMed Web of Science ®Google Scholar
• Yaylayan , V. A. 1997 . Classification of the Maillard reaction: A conceptual approach. . Trends Food Sci. Tech. , 8 : 13 – 18 .
   Web of Science ®Google Scholar
• Yeboah , F. K. and Yaylayan , V. A. 2001 . Analysis of glycated proteins by mass spectrometric techniques: Qualitative and quantitative aspects. . Nahrung , 3 : 164 – 171 .
   Google Scholar
• Yeboah , F. K. , Alli , I. , Yaylayan , V. A. , Konishi , Y. and Stefanowicz , P. 2000 . Monitoring glycation of lysozyme by electrospray ionization mass spectrometry. . J. Agric. Food Chem. , 48 : 2766 – 2774 .
   PubMedGoogle Scholar
• Yong , Y. H. and Foegeding , A. E. 2008 . Effects of caseins on thermal stability of β-lactoglobulin. . J. Agric. Food Chem. , 56 : 10352 – 10358 .
   PubMedGoogle Scholar
• Zhang , X. , Medzihradszky , K. F. , Cunningham , J. , Lee , P. D.K. , Rognerud , C. L. , Ou , C-N. , Harmatz , P. and Witkowska , H. E. 2001 . Characterization of glycated haemoglobin in diabetic patients: Usefulness of electrospray mass spectrometry in monitoring the extent and distribution of glycation. . J. Chromatogr. A , 759 : 1 – 15 .
   Google Scholar