[en] Isolated milk fat globules were subjected to enzyme hydrolysis by a specific protease (trypsin) and a nonspecific protease (pronase E) to study the asymmetric arrangement of milk fat globule membrane (MFGM) proteins. The remaining proteins on the globules after proteolysis were resolved by two-dimensional gel electrophoresis and identified by mass spectrometry. By this proteomic approach, the results confirmed different susceptibility of the MFGM proteins to proteolysis by enzymes. Butyrophilin and adipophilin were completely digested by trypsin and by pronase E, whereas lactadherin and xanthine dehydrogenase/oxidase were almost resistant to hydrolysis by trypsin and partially attacked by pronase E. Based on our results and recent bibliographic data, an up-dated model of the organization of some MFGM proteins is proposed and discussed. (c) 2011 Elsevier Ltd. All rights reserved.
Disciplines :
Food science
Author, co-author :
Vanderghem, Caroline ; Université de Liège - ULiège > Chimie et bio-industries > Chimie biologique industrielle
Francis, Frédéric ; Université de Liège - ULiège > Sciences agronomiques > Entomologie fonctionnelle et évolutive
Danthine, Sabine ; Université de Liège - ULiège > Chimie et bio-industries > Laboratoire des Sciences des aliments et formulation
Deroanne, Claude
Paquot, Michel ; Université de Liège - ULiège > Chimie et bio-industries > Chimie biologique industrielle
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)
Blecker, Christophe ; Université de Liège - ULiège > Chimie et bio-industries > Laboratoire des Sciences des aliments et formulation
Language :
English
Title :
Study on the susceptibility of the bovine milk fat globule membrane proteins to enzymatic hydrolysis and organization of some of the proteins
Aoki N. Regulation and functional relevance of milk fat globules and their components in the mammary gland. Bioscience Biotechnology Biochemistry 2006, 70:2019-2027.
Argento-Ceru M.P., Bargagli A.M., Sartori C. Topological location of diamine oxidase in the transverse plane of rabbit liver microsomal membranes. European Journal of Biochemistry 1984, 139:645-649.
Banghart L.R., Chamberlain C.W., Velarde J., Korobko I.V., Ogg S.L., Jack L.J., et al. Butyrophilin is expressed in mammary epithelial cells from a single-sized messenger RNA as a type I membrane glycoprotein. Journal of Biological Chemistry 1998, 273:4171-4179.
Bauer H. Ultrastructural observations on the milk fat globule envelope of cow's milk. Journal of Dairy Science 1972, 55:1375-1387.
Benoit B., Fauquant C., Daira P., Peretti N., Guichardant M., Michalski M.C. Phospholipid species and minor sterols in French human milks. Food Chemistry 2010, 120:684-691.
Brandt R., Pepperle M., Otto A., Kraft R., Boehmer F.D., Grosse R. A 13-kilodalton protein purified from milk fat globule membranes is closely related to a mammary-derived growth inhibitor. Biochemistry 1988, 27:1420-1425.
Brasaemle D.L. Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. Journal of Lipid Research 2007, 48:2547-2559.
Cavaletto M., Giuffrida M.G., Fortunato D., Gardano L., Dellavalle G., Napolitano L., et al. A proteomic approach to evaluate the butyrophilin gene family expression in human milk fat globule membrane. Proteomics 2002, 2:850-856.
Charlwood J., Hanrahan S., Tyldesley R., Langridge J., Dwek M., Camilleri P. Use of proteomic methodology for the characterization of human milk fat globular membrane proteins. Analytical Biochemistry 2002, 301:314-324.
Danthine S., Blecker C., Paquot M., Innocente N., Deroanne C. Evolution des connaissances sur la membrane du globule gras du lait: synthèse bibliographique. Lait 2000, 80:209-222.
Dewettinck K., Rombaut R., Thienpont N., Le T.T., Messens K., Van Camp J. Nutritional and technological aspects of milk fat globule membrane material. International Dairy Journal 2008, 18:436-457.
Evers J., Haverkamp R.G., Holroyd S.E., Jameson G.B., Mackenzie D.D.S., McCarthy O.J. Heterogeneity of milk fat globule membrane structure and composition as observed using fluorescence microscopy techniques. International Dairy Journal 2008, 18:1081-1089.
Evers J.M. The milk fat globule membrane-composition and structural changes post secretion by the mammary secretory cell. International Dairy Journal 2004, 14:661-674.
Fauquant C., Briard-Bion V., Leconte N., Guichardant M., Michalski M.C. Membrane phospholipids and sterols in microfiltered milk fat globules. European Journal of Lipid Science and Technology 2007, 109:1167-1173.
Fong B.Y., Norris C.S. Quantification of milk fat globule membrane proteins using selected reaction monitoring mass spectrometry. Journal of Agricultural and Food Chemistry 2009, 57:6021-6028.
Fong B.Y., Norris C.S., MacGibbon A.K.H. Protein and lipid composition of bovine milk-fat-globule membrane. International Dairy Journal 2007, 7:275-288.
Fortunato D., Giuffrida M.G., Cavaletto M., Garoffo L.P., Dellavalle G., Napolitano L., et al. Structural proteome of human colostral fat globule membrane proteins. Proteomics 2003, 3:897-905.
Gallier S., Gragson D., Jimenez-Flores R., Everett D.W. Using confocal laser scanning microscopy to probe the milk fat globule membrane and associated proteins. Journal of Agricultural and Food Chemistry 2010, 58:4250-4257.
Henson A.F., Holdsworth G., Chandan R.C. Physicochemical analyses of bovine milk fat globule membrane. II. Electron microscopy. Journal of Dairy Science 1971, 54:1752-1763.
Horisberger M., Rosset J., Vonlanthein M. Location of glycoproteins on milk fat globule membrane by scanning and transmission electron microscopy, using lectin-labelled gold granules. Experimental Cell Research 1977, 109:361-369.
Iman A. Investigation into the asymmetric distribution of proteins in human milk-fat-globule-membranes. Journal of Biochemistry 1986, 99:143-152.
Jenness R., Koops J. Preparation and properties of a salt solution which simulates milk ultrafiltrate. Netherlands Milk and Dairy Journal 1962, 16:153-164.
Keenan T.W. Assembly and secretion of the lipid globules of milk. Advanced Experimental Medical Biology 2001, 501:125-136.
Keenan T.W., Franke W.W., Kartenbeck J. Concanavalin A binding by isolated plasma membranes and endomembranes from liver and mammary gland. FEBS Letters 1974, 44:274-278.
Keenan T.W., Heid H.W., Stadler J., Jarasch E., Franke W.W. Tight attachment of fatty acids to proteins associated with milk lipid globule membrane. European Journal of Cell Biology 1982, 26:270-276.
Keenan T.W., Mather I.H. Intracellular origin of milk fat globules and the nature of the milk fat globule membrane. Advanced dairy chemistry. Lipids 2006, Vol. 2:137-171. Springer, New York, NY, USA. 3rd ed. P.F. Fox, P.L.H. McSweeney (Eds.).
Kobylka D., Carraway K.L. Proteolytic digestion of proteins of the milk fat globule membrane. Biochimica et Biophysica Acta 1973, 307:133-140.
Langen R., Isas J.M., Luecke H., Haigler H.T., Hubbell W.L. Membrane-mediated assembly of annexins studied by site-directed spin labeling. Journal of Biological Chemistry 1998, 273:22453-22457.
Lassen D., Lucke C., Kveder M., Mesgarzadeh A., Schmidt J.M., Specht B., et al. Three-dimensional structure of bovine heart fatty-acid-binding protein with bound palmitic acid, determined by multidimensional NMR spectroscopy. European Journal of Biochemistry 1995, 230:266-280.
Lopez C., Briard-Bion V., Menard O., Rousseau F., Pradel P., Besle J.M. Phospholipid, sphingolipid, and fatty acid compositions of the milk fat globule membrane are modified by diet. Journal of Agricultural and Food Chemistry 2008, 56:5226-5236.
Lopez C., Madec M.N., Jimenez-Flores R. Lipid rafts in the bovine milk fat globule membrane revealed by the lateral segregation of phospholipids and heterogeneous distribution of glycoproteins. Food Chemistry 2010, 120:22-33.
McManaman J.L., Zabaronick W., Schaack J., Orlicky D.J. Lipid droplet targeting domains of adipophilin. Journal of Lipid Research 2003, 44:668-673.
McPherson A.V., Kitchen B.J. Reviews of the progress of dairy science: the bovine milk fat globule membrane- its formation, composition, structure and behaviour in milk and dairy products. Journal of Dairy Research 1983, 50:107-133.
Makowski L., Hotamisligil G.S. Fatty acid binding proteins - the evolutionary crossroads of inflammatory and metabolic responses. Journal of Nutrition 2004, 134:2464S-2468S.
Mather I.H. A review and proposed nomenclature for major proteins of the milk-fat globule membrane. Journal of Dairy Science 2000, 83:203-247.
Mather I.H., Keenan T.W. Studies on the structure of milk fat globule membrane. Journal of Membrane Biology 1975, 21:65-85.
Mather I.H., Weber K., Keenan T.W. Membranes of mammary gland. XII. Loosely associated proteins and compositional heterogeneity of bovine milk fat globule membrane. Journal of Dairy Science 1977, 60:394-402.
Michalski M.-C. Specific molecular and colloidal structures of milk fat affecting lipolysis, absorption and postprandial lipemia. European Journal of Lipid Science and Technology 2009, 111:413-431.
Michalski M.-C., Briard V., Michel F., Tasson F., Poulain P. Size distribution of fat globules in human colostrum, breast milk, and infant formula. Journal of Dairy Science 2005, 88:1927-1940.
Michalski M.-C., Soares A.F., Lopez C., Leconte N., Briard V., Geloen A. The supramolecular structure of milk fat influences plasma triacylglycerols and fatty acid profile in the rat. European Journal of Nutrition 2006, 45:215-224.
Nielsen C.S., Bjerrum O.J. Crossed immunoelectrophoresis of bovine milk fat globule membrane protein solubilized with non-ionic detergent. Biochimica et Biophysica Acta 1977, 466:496-509.
Patton S., Trams E.G. The presence of plasma membrane enzymes on the surface of bovine milk fat globules. FEBS Letters 1971, 14:230-232.
Peterson J.A., Hamosh M., Scallan C.D., Ceriani R.L., Henderson T.R., Mehta N.R., et al. Milk fat globule glycoproteins in human milk and in gastric aspirates of mother's milk-fed preterm infants. Pediatric Research 1998, 44:499-506.
Quaranta S., Giuffrida M.G., Cavaletto M., Giunta C., Godovac-Zimmermann J., Canas B., et al. Human proteome enhancement: high-recovery method and improved two-dimensional map of colostral fat globule membrane proteins. Electrophoresis 2001, 22:1810-1818.
Rasmussen J.T. Bioactivity of milk fat globule membrane proteins. Australian Journal of Dairy Technology 2009, 64:63-67.
Reinhardt T.A., Lippolis J.D. Bovine milk fat globule membrane proteome. Journal of Dairy Research 2006, 73:406-416.
Reinhardt T.A., Lippolis J.D. Developmental changes in the milk fat globule membrane proteome during the transition from colostrum to milk. Journal of Dairy Science 2008, 91:2307-2318.
Rescher U., Gerke V. Annexins-unique membrane binding proteins with diverse functions. Journal of Cell Science 2004, 117:2631-2639.
Robenek H., Hofnagel O., Buers I., Lorkowski S., Schnoor M., Robenek M.J., et al. Butyrophilin controls milk fat globule secretion. Proceedings of the National Academy of Science USA 2006, 103:10385-10390.
Sanchez-Juanes F., Alonso J.M., Zancada L., Hueso P. Distribution and fatty acid content of phospholipids from bovine milk and bovine milk fat globule membranes. International Dairy Journal 2009, 19:273-278.
Shimizu M., Kanno C., Yamauchi K. Selective solubilization of bovine milk fat globule membrane proteins with guanidine hydrochloride and disposition of some of the proteins. Agricultural and Biological Chemistry 1978, 42:2309-2314.
Shimizu M., Yamauchi K., Kanno C. Proteolytic digestion of milk fat globule membrane proteins. Milchwissenschaft 1979, 34:666-668.
Silanikove N., Shapiro F. Distribution of xanthine oxidase and xanthine dehydrogenase activity in bovine milk: physiological and technological implications. International Dairy Journal 2007, 17:1188-1194.
Smolenski G., Haines S., Kwan F.Y., Bond J., Farr V., Davis S.R., et al. Characterisation of host defence proteins in milk using a proteomic approach. Journal of Proteome Research 2007, 6:207-215.
Sorensen E.S., Rasmussen L.K., Moller L., Petersen T.E. The localization and multimeric nature of component PP3 in bovine milk: purification and characterization of PP3 from caprine and ovine milks. Journal of Dairy Science 1997, 80:3176-3181.
Spitsberg V.L., Matitashvili E., Gorewit R.C. Association and coexpression of fatty-acid-binding protein and glycoprotein CD36 in the bovine mammary gland. European Journal of Biochemistry 1995, 230:872-878.
Takai Y., Sasaki T., Matozaki T. Small GTP-binding proteins. Physiological Reviews 2001, 81:153-208.
Vanderghem, C. (2009). The milk fat globule membrane: physico-chemical studies and its techno-functional valorisation in buttermilk. PhD Thesis. Gembloux Agro-Bio Tech, University of Liège.
Vanderghem C., Blecker C., Danthine S., Deroanne C., Haubruge E., Guillonneau F., et al. Proteome analysis of the bovine milk fat globule: enhancement of membrane purification. International Dairy Journal 2008, 18:885-893.
Vanderghem C., Bodson P., Danthine S., Paquot M., Deroanne C., Blecker C. Milk fat globule membrane and buttermilks: from composition to valorization. Biotechnologie, Agronomie, Société et Environnement 2010, 14:485-500.
Wagner J.A., Kelly R.B. Topological organization of proteins in an intracellular secretory organelle: the synaptic vesicle. Proceedings of the National Academy of Science USA 1979, 76:4126-4130.
Wooding F.B. The structure of the milk fat globule membrane. Journal of Ultrastructure Research 1971, 37:388-400.
Wooding F.B.P. Milk fat globule membrane material in skim-milk. Journal of Dairy Research 1974, 41:331-337.
