Thermal Aggregation of Whey Proteins in Model Solutions as Affected by Casein/Whey Protein Ratios
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1 JOURNAL OF FOOD SCIENCE FOOD CHEMISTRY AND TOXICOLOGY Thermal Aggregation of Whey Proteins in Model Solutions as Affected by Casein/Whey Protein Ratios M. Beaulieu, Y. Pouliot, and M. Pouliot ABSTRACT Model solutions (32.5 g protein/l) prepared from milk, ultrafiltration permeate, and whey protein isolate were adjusted at ph 6.7 to casein:whey protein (C:W) ratios of 80:20, 60:40, 40:60, 20:80, and 0:100. Heating was performed in test tubes at 95 C for 5 min. Observations of the heated suspensions revealed the occurrence of heterogeneous particulates from the existing casein micelles complexed with denatured whey proteins and from aggregates essentially consisting of denatured whey proteins. The proportion of whey protein aggregates increased as C:W was changed from 80:20 to 20:80. The results from this study confirmed that heat-induced aggregates were formed not only from casein micelles but also from heat-denatured whey proteins. Keywords: heat treatment, casein, whey protein, aggregates, microscopy INTRODUCTION HEAT TREATMENTS IN THE RANGE 70 TO 140 C ARE WIDELY USED as unit operations in the processing of liquid milk or milk products to reduce bacterial counts, extend shelf life, and/or generate changes in rheological properties, such as in yogurt (Jelen and Rattray, 1995). Several commercial dairy-based products are being developed by modifying the casein:whey protein (C:W) ratio of milk, using whey proteins as ingredients (Jelen, 1992). The manipulation of the C:W ratio in milk influences its heat stability (Singh and Fox, 1987; Patocka et al.,1993), but little is known about the effects of this modification on heat-induced aggregation of whey proteins. Heating casein micelles below 140 C has little effect on their stability and stucture (Fox, 1982). However, heat treatment induces changes in the structure of whey proteins (Dannenberg and Kessler, 1988; Parris et al., 1991; Qi et al., 1995; Jelen and Rattray, 1995), leading to irreversible denaturation. The rate and the extent of whey protein denaturation are affected by environmental conditions (Dannenberg and Kessler, 1988); this relationship has been proposed as responsible for the ph-dependency of heat stability in milk (Singh and Fox, 1985 and 1986; Singh and Creamer, 1992; Singh et al., 1996). Heating milk above 70 C predominantly induces the denaturation of whey proteins and their complex formation with casein micelles involving k-casein (Rose, 1963; Creamer et al, 1978; Singh and Fox, 1985; Dannenberg and Kessler, 1988; Dalgleish, 1990; Singh and Latham, 1993). Smits and van Brouwershaven (1980) showed that up to 80% of b-lactoglobulin (b-lg) could be complexed to casein micelles after a heat treatment of 90 C for 20 min. The complex between b-lg and k-casein involves disulfide bonds (Jang and Swaisgood, 1990), and its formation is dependent on the temperature and ph of heating (Singh and Fox, 1987; Dannenberg and Kessler, 1988). Singh and Fox (1987) reported that complex formation with b-lg appeared to The authors are affiliated with the Centre de recherche STELA, Université Laval, Québec, Canada, G1K 7P4. Address inquiries to Dr. M. Beaulieu. ( marbeau@globetrotter.qc.ca). prevent the dissociation of micellar k-casein on heating and stabilized the micelles in the ph range 6.5 to 6.7. However, at ph 6.9, k- casein/b-lg complexes dissociated from the micelles on heating. They also reported that high concentrations of b-lg ( 8 g/l) induced coagulation at ph 7.3, essentially by promoting the dissociation of micellar k-casein. Very few studies that are related to the effect of C:W ratios on the heat-induced denaturation/aggregation of whey proteins have been published. Corredig and Dalgleish (1996) quantified the amount of a- lactalbumin (a-la) and b-lg complexed to casein micelles upon adding native a-la or b-lg to skim milk prior to heating at 80 C for up to 80 min (ph 8.0). They reported a plateau value in the amount of a-la and b-lg (up to 0.8 mg/mg k-casein ) that could be complexed with micellar k-casein. Adding excess a-la and b-lg affected the kinetics of heat denaturation but not the maximum value which corresponded to that of skim milk. Their observations suggest that heating casein micelles in the presence of excessive proportions of whey proteins may lead to self-aggregation of b-lg and a-la and potentially generate whey protein complexes. Changes in the total protein content affect the kinetics of heat denaturation as well as the type of aggregation in a complex protein system. Our objective was to investigate the effects of C:W ratios, over the range 80:20 to 0:100, on the heat-induced aggregation/ denaturation of whey proteins in model systems. Protein content and mineral distribution were kept constant at all ratios. A heat treatment of 95 C for 5 min was applied in order to represent a common timetemperature combination used as the pre-heating step in the processing of retort-sterilized products. MATERIALS & METHODS Preparation of model solutions Raw milk (Ferme SMA, Quebec, Canada) was carefully skimmed by double-centrifugation at 3000 g for 5 min at 4 C. Ultrafiltration permeate was obtained by filtration at 25 C with a polysulfone membrane of 10 kda cut-off (Romicon PM 10, Woburn, Mass., U.S.A.). Model solutions (32.5 g/l total protein) were prepared by mixing skim milk, its UF-permeate, and industrial whey protein isolates (940 g protein/kg dry powder) (Le Sueur Isolates, Le Sueur, Minn., U.S.A.) to provide C:W ratios of 80:20, 60:40, 40:60, 20:80, and 0:100. NaN 3 (0.2 g/l) was added to prevent microbial growth. The ph was adjusted to 6.7 with 1 M HCl and time was allowed to reach equilibrium. Model solutions were made in triplicate with three lots of milk. Heat treatment Samples were heated in closed test tubes immersed in a water bath at C. The tubes were held 5 min after reaching 95 C and then cooled rapidly to room temperature in cold water. Temperature increase was measured with a thermometer, and 95 C was reached in 5 min. Centrifugation To facilitate the investigation on the extent of denaturation of whey proteins, of their association with the casein micelles, and of the size distribution of aggegates after heating, solutions were centrifuged at 776 JOURNAL OF FOOD SCIENCE Volume 64, No. 5, Institute of Food Technologists
2 3000 g for 60 min at 4 C to separate larger aggregates from the solution. Centrifugation conditions had been determined from preliminary experiments designed to obtain reliable material for particle size determination. Polyacrylamide gel electrophoresis Pellets, supernatants, and uncentrifuged solutions of raw and heated samples were analyzed by SDS-PAGE using the method of Laemmli (1970), in which separating gels were composed of 150 g/l acrylamide in Tris/HCl buffer, ph 8.8, and the stacking gels contained 40 g/l acrylamide in Tris/HCl buffer, ph 6.8 (Singh and Creamer, 1991). The gels were stained with Coomassie Blue in isopropanol, acetic acid, and water (25:10:65 by volume). Table 1 Soluble proteins (ph 4.6) before and after heating model solutions at 95 C for 5min a Content in soluble whey proteins (g/l) Ratio b-lactoglobulin a-lactalbumin BSA (C:W) Unheated Heated Unheated Heated Unheated Heated 80: nd nd 60: nd nd 40: nd nd 20: nd nd 0: nd nd absa=bovine Serum Albumin; nd=not detectable Reversed-phase HPLC of soluble whey proteins Reversed-phase chromatography separation (RP-HPLC) was performed on a C 4 Vydac 214TP column installed on a Waters HPLC (model 600E, Milford, Mass., U.S.A.), equipped with an UV detector (model 486, Waters), a manual injection system (model 7725i, Rheodyne, Cotati, Calif., U.S.A.) and controlled by Millenium Software (Waters). The method was standardized with pure protein samples from Sigma Chemical Company (St Louis, Mo., U.S.A.) and the calibration enabled evaluation of concentrations with a coefficient of variation of 7%. Samples were adjusted to ph 4.6, centrifuged and filtered on a 0.2- m filter prior to injection. Particle size determination The size distributions of protein aggregates were determined by photon correlation spectroscopy (PCS). Measurements were taken using the Nicomp multibit (7 bits) 64-channel photon correlation system (Model 370, Pacific Scientific, Hiac/Royce Instruments Division, Menlo Park, Calif., U.S.A.). Correlation functions were applied to the light scattered at an angle of 90 by the particles in suspension. Protein solutions were dispersed in a buffer containing 5 mm CaCl 2, 20 mm imidazole, and 50 mm NaCl, ph 6.7 (Dalgleish and Banks, 1991). Three measurements of the size distribution of the protein aggregates were made on each sample. lg, 1.05 to 4.29 g/l for a-la, and 0.14 to 0.62 g/l for BSA, as the C:W ratios were modified from 80:20 to 0:100. Discrepancies between soluble and total whey proteins were due to the nature of the whey protein source and RP-HPLC sample preparations. Whey protein isolates (WPI) are not completely free from denatured and complexed proteins that would be removed during sample preparation for analysis. No detectable amounts of b-lg and BSA remaining soluble after heat treatment were found at any C:W ratio. In contrast, residual amounts of soluble a-la were found and decreased from 0.45 g/l to 0.18 g/l as the proportion of whey proteins in the model solutions was increased. The decrease in soluble a-la after heating with increasing whey protein content was not linear. The patterns from SDS-PAGE of heated solutions (Fig. 1) confirmed the extensive denaturation of whey proteins. The absence of Embedding of milk protein solutions Raw and heated solutions were poured into small agar (50 g/l) microcapsules (Salyaev, 1968) and fixed a first time with glutaraldehyde (30 ml/l) and paraformaldehyde (20 ml/l) in a cacodylate buffer (0.1 M, ph 7.4). A second fixation was done with 10 g/l osmium tetraoxide (OsO 4 ) in the same buffer. Samples were then dehydrated in a graduated ethanol and propylene oxide series prior to embedding in Epon 812 resin. Marking of thin sections of milk protein solutions Fresh thin sections of the embedded samples were successively floated in Tris-HCl buffer (0.1 M, ph 7.2) containing: (a) 50 g/ml Limax Flavus agglutinin (LFA), which is specific to sialic acid located on the C-terminal portion of k-casein (45 min at 37 C), and (b) fetuin/ gold complexes 15 nm (45 min at 37 C). The grids were washed 3 times (2 min) with the Tris-HCl buffer after each step. Control experiments were performed in the absence of casein, LFA, and fetuin. Transmission electron microscopy Thin sections were stained with 10 g/l uranyl acetate and lead citrate (Reynolds, 1963). All preparations were examined on a Jeol 1200 EX transmission electron microscope. At least 3 pictures were randomly taken on each section. RESULTS Heat denaturation of whey proteins The amount of soluble whey proteins, determined in model solutions before heating, increased (Table 1) from 3.71 to g/l for b- Fig. 1 SDS-PAGE patterns of model solutions (lanes 1 to 5) and supernatants (lanes 6 to 10) obtained before (a) and after (b) heating step, presented in the following order of casein:whey protein ratios: 80:20, 60:40, 40:60, 20:80, 0:100. Volume 64, No. 5, 1999 JOURNAL OF FOOD SCIENCE 777
3 Casein:Whey Protein Aggregates... sharp bands in the area of BSA, b-lg, and a-la revealed some denaturation of those proteins. Note also that the amount of material in the wells increased with increasing proportions of whey proteins in the heated solutions, suggesting that large and/or insoluble protein aggregates were present in heated solutions. Centrifugal separation of the aggregated material enabled the removal of insoluble material that could not be dissociated with our SDS-PAGE sample buffer and further analyzed. However, the SDS-PAGE gels of the supernatants of heated solutions (Fig. 1) showed a decreasing intensity of bands compared to those of native solutions, for the same quantity of sample loaded in the wells, suggesting that proteinaceous material was removed by centrifugation. These observations confirmed RP-HPLC results. Effect of C:W ratios on particle sizes in heated solutions The average volume-weighted diameter was determined (Fig. 2) on model solutions and on supernatant, before and after heating. An average diameter of 135 nm was found with the C:W 80:20 solution, representing the typical size of casein micelles in raw skim milk, whereas its supernatant showed a higher value at 240 nm. Increasing the proportion of whey proteins in model solutions had little effect ( 10 nm) on the average particle diameters of the solutions before heating, but values decreasing from 240 to 195 nm were found from the supernatant. Some remaining milk fat globules could explain the higher diameter values for the supernatant. In fact, large-size particles greatly affect PCS signal. Heating skim milk shifted the average diameter to 145 nm and that of the centrifuged material to 300 nm. The increases in diameter of the particles upon heating became more important as the whey protein proportion increased. For example, a shift from 125 to 340 nm was found on the C:W 40:60 solution, and from 240 to 460 nm on its supernatant. Reliable results could hardly be obtained with samples at highest whey protein proportions (20:80 and 0:100), presumably due to the polydispersity of the particles. Microstructure of colloidal particles and -casein localization Electron micrographs of casein micelles in unheated model solution (Fig. 3a) revealed the presence of well-defined particles with a sharp contour. Gold-labeling of the micrographs confirmed the occurrence of k-casein among the colloidal structure (Fig. 3c). The distribution of the gold granules, in the largest particles, appeared to be mainly peripheral. However, note that observations were made on casein micelle thin cuts. This implies that we could observe either casein micelle surface (pronounced labeling) or casein micelle center (weak labeling). When skim milk (C:W 80:20) was heated, a diffuse layer could be observed around the casein micelles but no loose material could be seen in the background (Fig. 3b). With the increase of whey protein proportion, the background of micrographs from heated samples (Fig. 4) became more reticulated, and irregularly shaped particles appeared. After the heat treatment, a greater proportion of particles were not gold-labeled. Gold-labeling of the background of micrographs from samples containing casein was generally more important than that observed in samples containing only whey proteins, suggesting that dissociated k-casein could be present in the solutions. Some background signal was observed in all micrographs, but in no instance did it overcome the specific labeling of the k-casein. DISCUSSION THE COMPLETE DENATURATION OF b-lg AND BSA AFTER 95 C FOR 5 min was consistent with known kinetics of denaturation of whey protein fractions (Dannenberg and Kessler, 1988; Jelen and Rattray, 1995). The occurrence of residual a-la can, however, be explained by differences in denaturation rate between whey protein fractions. According to Corredig and Dalgleish (1996), b-lg reacts at a much faster rate than a-la with casein micelles at 90 C. In addition, higher b-lg concentrations, as in our solutions, could result in increased rates of aggregation (Nielsen et al., 1996) and amplify differences in denaturation rates. However, higher concentrations of all whey proteins lead to greater thermal denaturation of a-la (Hines and Foegeding, 1993). The presence of b-lg accelerates the aggregation of a-la, which also becomes irreversible (Corredig and Dalgleish, 1996). Complex formation of whey proteins with casein micelles is limited to a plateau value, as suggested by Corredig and Dalgleish (1996). They estimated the sum of the molar ratios of b-lg and a-la bound to micellar casein to be 1.5 mole whey proteins/mole of k-casein. After adding 2 mg/ml of b-lg in a standard milk (equivalent of a 75:25 ratio), the a-la reaction at 80 C was faster in the presence of b-lg. The a-la/k-casein ratio, however, reached the same plateau value as the control (Corredig and Dalgleish, 1996). The same observations were made for the b-lg. This result suggested that the plateau value was due to the saturation of k-casein. The ratios we used generated supersaturation with respect to whey proteins. Our results from the determina- a b c Fig. 2 Volume-weighted average diameter (Dv) of model solutions ( ) and of supernatants ( ) before (, ) and after (, ) heating at 95 C for 5min. Fig. 3 Transmission electron micrographs of model solutions with casein:whey protein ratio of 80:20 : (a) unheated, (b) heated, and (c) gold-labeled (scale bar=200nm). 778 JOURNAL OF FOOD SCIENCE Volume 64, No. 5, 1999
4 tion of soluble proteins after heating could suggest that all the whey proteins were complexed to the casein micelles. On the other hand, PCS results and TEM micrographs strongly suggest the saturation of casein micelles with whey proteins and the formation of additional whey protein aggregates. The increase in particle size upon heating milk has been reported (Hostettler et al., 1965; Mohammad and Fox, 1987; Dalgleish et al., 1987). This increase is typically related to the aggregation of whey proteins at the surface of casein micelles via the b-lg/k-casein complexes and disulfide-linked aggregates between k-casein and whey proteins (Singh and Latham, 1993). In our results, as the proportion of whey proteins was increased, we observed an increase in size of the aggregates. However, at C:W 60:40 and higher, the size distribution of the aggregates became heterogeneous, and we could not obtain reliable PCS measurements. The electron micrographs confirmed that large and irregularly shaped particles were formed upon heating. Solutions with a whey protein proportion greater than 40 mainly generated whey protein aggregates. Results from RP-HPLC and SDS-PAGE analyses showed that high-molecular-weight aggregates were formed during heating of model solutions. The size and composition of these aggregates could not be established from our results but Singh and Latham (1993) stated that large aggregates (mol wt 1 106) composed of k-casein, b-lg, and a-la could be formed during heating skim milk at 140 C for more than 2 min (ph 6.67). An intermediate fraction of 100,000 to 600,000 mol wt was also present in their heated samples. Other work on the a b protein heat denaturation in skim milk (Dalgleish, 1990) showed that large aggregates were formed even when the extent of denaturation was relatively small. Singh et al. (1996) reported that the amount of whey proteins associated with the casein micelles were lower than the amounts denatured. For example, 74% of b-lg was denatured after a heat treatment of 80 C for 5 min, but only 58% was associated with casein micelles. Our results confirmed their findings and suggest that the complexation of whey proteins did not only occur via the b-lg/k-casein interaction but that a-la/a-la, b-lg/b-lg, and b-lg/a-la complex formation could also be responsible for changes in soluble proteins during the heating of complex systems. These agregates could be observed and the fact that they were unlabeled confirmed their whey protein content (Fig. 4). Our results from PCS analyses and TEM observations suggested a limitation in the size increase of aggregates as a result of whey proteins directly taken up by casein micelles. Researchers (Dalgleish, 1990; Singh and Latham, 1993) have shown that particles formed by the aggregation of whey proteins on casein micelles did not form infinite aggregates and that their size was limited by the amount of k- casein present in the system during heating. This suggests that whey proteins present in excess proportion could lead to whey protein selfaggregation. Electron microscopy studies showed that high heat treatment of milk not only increased the size of the casein micelles (Creamer et al., 1978; Mohammad and Fox, 1987) but also increased the number of protein particles smaller than casein micelles. Some of these smaller particles were composed of heat-denatured whey proteins that were not attached to the micelles and of soluble casein formed by dissociation of micelles (Morr, 1969; Aoki et al., 1974). TEM micrographs (Fig. 4) strongly confirmed this view. The occurrence of colloidal gold granules in the background of TEM micrographs containing caseins may suggest that some of the whey protein/k-casein complexes were formed in the serum. About 10% of k-casein in unheated milk was present in the serum and could react with denatured whey proteins. Singh and Latham (1993) had estimated that about 10% to 15% of the total whey protein/k-casein complexes remained in the supernatant during extended heating. However, most ( 90%) of the total WP/k-CN formed complexes that remained attached to the casein micelles when heating had been at or below ph 6.7. c Fig. 4 Transmission electron micrographs of model solutions heated and gold-labeled for casein:whey protein ratios (a) 60:40, (b) 40:60, (c) 20:80, and (d) 0:100 (scale bar=200 nm). d CONCLUSION OUR RESULTS CONFIRMED THAT THE PROPORTION OF WHEY PROteins in the heated solutions had an important effect on the formation of aggregates. Higher whey protein concentrations led to the formation of new particles mainly composed of whey proteins. There is a need to investigate further the impact of such aggregation on the heat stability of systems with modified casein:whey protein ratios. REFERENCES Aoki, T., Susuki, H., and Imamura, T Formation of soluble casein in whey protein-free milk heated at high temperature. Milchwissenschaft 29: Corredig, M. and Dalgleish, D.G Effect of temperature and ph on the interactions of whey proteins with casein micelles in skim milk. Food Research International 1: Creamer, L.K., Berry, G.P., and Matheson, A.R The effect of ph on protein aggregation in heated skim milk. N. Z. J. Dairy Sci. Technol. 13: Dalgleish, D.G Denaturation and aggregation of serum proteins and caseins in heated milk. J. Agric. Food Chem. 38: Dalgleish, D.G. and Banks, J.M The formation of complexes between serum proteins and fat globules during heating of whole milk. Milchwissenschaft 46: Dalgleish, D.G., Pouliot, Y., and Paquin, P Studies on the stability of milk. II. Association and dissociation of particules and the effect of added urea. J. Dairy Res. 54: Dannenberg, F. and Kessler, H.G Reaction kinetics of the denaturation of whey proteins in milk. J. Food Sci. 53: Fox, P.F Heat-induced coagulation of milk. Ch. 6 in Developments in Dairy Chemistry-1, P.F. Fox (Ed.), p Applied Science Publishers, London. Hines, M.E. and Foegeding, E.A Interactions of a-lactalbumin and bovine serum albumin with b-lactoglobulin in thermally induced gelation. J. Agric. Food Chem. 41: Hostettler, H., Imhof, K., and Stein, J Studies on the effect of heat-treatment and lyophilisation on the state of distribution and physiological properties of milk proteins with special consideration of heat-treatment conditions applied in uperization. I. Effect on the state of distribution of protein. Milchwissenschaft 20: Volume 64, No. 5, 1999 JOURNAL OF FOOD SCIENCE 779
5 Casein:Whey Protein Aggregates Jang, H.D. and Swaisgood, H.E Disulfide bond formation between thermally denatured b-lactoglobulin and k-casein micelles. J. Dairy Sci. 73: Jelen, P Heat stability of dairy systems with modified casein-whey protein content. Section 4.1 in Protein and Fat Globule Modifications by Heat Treatment, Homogenization and Other Technological Means for High Quality Dairy Products, p International Dairy Federation, Brussels, Belgium. Jelen, P. and Rattray, W Ch. 4, p in Heat-Induced Changes in Milk. 2nd ed., International Dairy Federation, Brussels, Belgium. Laemmli, U.K Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277: Mohammad, K.S. and Fox, P.F Heat-induced microstructural changes in casein micelles before and after heat coagulation. N. Z. J. Dairy Sci. Technol. 22: Morr, C.V Protein aggregation in conventional and ultra-high-temperatureheated skim milk. J. Dairy Sci. 52: Nielsen, B.T., Singh, H., and Latham, J.M Aggregation of bovine b-lactoglobulin A and B on heating at 75 C. Int. Dairy J. 6: Parris, N., Purcell, J.M., and Ptashkin, S.M Thermal denaturation of whey proteins in skim milk. J. Agric. Food Chem. 39: Patocka, G., Jelen, P., and Kalab, M Thermostability of skimmilk with modified casein/whey protein content. Int. Dairy J. 3: Qi, X.L., Brownlow, S., Holt, C., and Sellers, P Thermal denaturation of b-lactoglobulin: effect of protein concentration at ph 6.75 and Biochimica et Biophysica Acta 1248: Reynolds, E.S The use of lead citrate at high ph as an electron opaque stain in electron microscopy. J. Cell Biol. 17: Rose, D Heat stability of bovine milk: a review. Dairy Science Abstracts 52: Salyaev, R.K A method of fixation and embedding of liquid and fragile materials in agar microcapsulae. Fourth European Regional Conference on Electron Microscopy, Volume II. Daria Steve Bocciarelli (Ed.), p Rome, Italy. Singh, H. and Creamer, L.K Aggregation and dissociation of milk protein complexes in heated reconstituted concentrated skim milk. J. Food Sci. 56: Singh, H. and Creamer, L.K Ch. 15, p , in Advanced Dairy Chemistry, Volume I, Proteins. Elsevier Science Publishers, Barking, UK. Singh, H. and Fox, P.F., Heat stability of milk: ph-dependent dissociation of micellar k-casein on heating milk at ultra-high temperatures. J. Dairy Res. 52: Singh, H. and Fox, P.F Heat stability of milk: further studies on the ph-dependent dissociation of micellar k-casein. J. Dairy Res. 53: Singh, H. and Fox, P.F Heat stability of milk: Role of b-lactoblobulin in the phdependent dissociation of micellar k-casein. J. Dairy Res. 54: Singh, H. and Fox, P.F Heat stability of milk: ph-dependent dissociation of micellar k-casein on heating milk at ultra high temperatures. J. Dairy Res. 59: Singh, H. and Latham, J.M Heat stability of milk: aggregation and dissociation of protein at ultra-high temperatures. Int. Dairy J. 3: Singh, H., Roberts, M.S., Munro, P.A., and Teo, C.T Acid-induced dissociation of casein micelles in milk: effects of heat treatment. J. Dairy Sci. 79: Smits, P. and van Brouwershaven, J.H Heat-induced association of b-lactoglobulin and casein micelles. J. Dairy Res. 47: MS 4298; received 10/3/98; revised 1/23/99; accepted 3/23/99. We thank Alain Goulet for his contribution in the preparation and use of gold-labeling and in the performance of electron microscopy. This project was partly supported by the Natural Sciences & Engineering Research Council of Canada (NSERC). 780 JOURNAL OF FOOD SCIENCE Volume 64, No. 5, 1999
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