Impact of the dairy product structure and protein nature on the proteolysis and amino acid bioaccessiblity during in vitro digestion

Food Hydrocolloids

Volumn 82, Issue , 2018, Pages 399-411

  Lorieau, L ^a   Halabi, A ^a   Ligneul, A ^b   Hazart, E ^b   Dupont, D ^a   Floury, J ^a  

^a AGROCAMPUS OUEST   (France)

^b LACTALIS Recherche et Développement   (France)

Author keywords

Amino acids; Bioaccessibility; Dairy gel; Digestion; Heat treatment; Whey proteins

Indexed keywords

AMINO ACIDS; BIOSYNTHESIS; CASEIN; EMULSIFICATION; GELATION; HEAT TREATMENT; HYDROLYSIS; PROTEOLYSIS; TEXTURES;

AMINO-ACIDS; BIOACCESSIBILITY; DAIRY GEL; DIGESTION; ELDERLY PEOPLE; IN-VITRO DIGESTIONS; PERFORMANCE; PRODUCT STRUCTURE; PROTEIN HYDROLYSIS; WHEY PROTEINS;

GELS;

EID: 85047481369     PISSN: 0268005X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodhyd.2018.04.019     Document Type: Article

References (56)

1. Asselin, J., Hébert, J., Amiot, J., Effects of in vitro proteolysis on the allergenicity of major whey proteins. Journal of Food Science 54:4 (1989), 1037–1039, 10.1111/j.1365-2621.1989.tb07938.x.
2. Awati, A., Rutherfurd, S.M., Kies, A.K., Veyry, A., Moughan, P.J., Endogenous lysine in ileal digesta in the growing rat determined using different methods. Journal of the Science of Food and Agriculture 89:13 (2009), 2200–2206, 10.1002/jsfa.3706.
3. Barbé, F., Le Feunteun, S., Rémond, D., Ménard, O., Jardin, J., Henry, G., Dupont, D., Tracking the in vivo release of bioactive peptides in the gut during digestion: Mass spectrometry peptidomic characterization of effluents collected in the gut of dairy matrix fed mini-pigs. Food Research International 63:Part B (2014), 147–156, 10.1016/j.foodres.2014.02.015.
4. Barbé, F., Ménard, O., Le Gouar, Y., Buffière, C., Famelart, M.-H., Laroche, B., Rémond, D., The heat treatment and the gelation are strong determinants of the kinetics of milk proteins digestion and of the peripheral availability of amino acids. Food Chemistry 136:3–4 (2013), 1203–1212, 10.1016/j.foodchem.2012.09.022.
5. Bendtsen, L.Q., Lorenzen, J.K., Bendsen, N.T., Rasmussen, C., Astrup, A., Effect of dairy proteins on appetite, energy expenditure, body weight, and composition: A review of the evidence from controlled clinical trials. Advances in Nutrition: An International Review Journal 4 (2013), 418–438, 10.3945/an.113.003723.
6. Bohn, T., Carriere, F., Day, L., Deglaire, A., Egger, L., Freitas, D., Dupont, D., Correlation between in vitro and in vivo data on food digestion. What can we predict with static in vitro digestion models?. Critical Reviews in Food Science and Nutrition 0:0 (2017), 1–23, 10.1080/10408398.2017.1315362.
7. Boirie, Y., Dangin, M., Gachon, P., Vasson, M.P., Maubois, J.L., Beaufrère, B., Slow and fast dietary proteins differently modulate postprandial protein accretion. Proceedings of the National Academy of Sciences of the United States of America 94:26 (1997), 14930–14935.
8. Borreani, J., Llorca, E., Quiles, A., Hernando, I., Designing dairy desserts for weight management: Structure, physical properties and in vitro gastric digestion. Food Chemistry 220:Supplement C (2017), 137–144, 10.1016/j.foodchem.2016.09.202.
9. Buse, M.G., Reid, S.S., Leucine. A possible regulator of protein turnover in muscle. Journal of Clinical Investigation 56:5 (1975), 1250–1261.
10. Chelh, I., Gatellier, P., Santé-Lhoutellier, V., Technical note: A simplified procedure for myofibril hydrophobicity determination. Meat Science 74:4 (2006), 681–683 https://doi.org/10.1016/j.meatsci.2006.05.019.
11. Church, F.C., Swaisgood, H.E., Porter, D.H., Catignani, G.L., Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. Journal of Dairy Science 66:6 (1983), 1219–1227 https://doi.org/10.3168/jds.S0022-0302(83)81926-2.
12. Cuthbertson, D., Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. The FASEB Journal, 2004 https://doi.org/10.1096/fj.04-2640fje.
13. Dangin, M., Boirie, Y., Garcia-Rodenas, C., Gachon, P., Fauquant, J., Callier, P., Beaufrère, B., The digestion rate of protein is an independent regulating factor of postprandial protein retention. American Journal of Physiology. Endocrinology and Metabolism 280:2 (2001), E340–E348.
14. Fang, X., Rioux, L.-E., Labrie, S., Turgeon, S.L., Commercial cheeses with different texture have different disintegration and protein/peptide release rates during simulated in vitro digestion. International Dairy Journal 56 (2016), 169–178 https://doi.org/10.1016/j.idairyj.2016.01.023.
15. Floury, J., Bianchi, T., Thévenot, J., Dupont, D., Jamme, F., Lutton, E., Le Feunteun, S., Exploring the breakdown of dairy protein gels during in vitro gastric digestion using time-lapse synchrotron deep-UV fluorescence microscopy. Food Chemistry 239 (2018), 898–910 https://doi.org/10.1016/j.foodchem.2017.07.023.
16. Fontana, A., Polverino de Laureto, P., De Filippis, V., Scaramella, E., Zambonin, M., Probing the partly folded states of proteins by limited proteolysis. Folding & Design 2:2 (1997), R17–R26 https://doi.org/10.1016/S1359-0278(97)00010-2.
17. Gornall, A.G., Bardawill, C.J., David, M.M., Determination of serum proteins by means of the Biuret reaction. Journal of Biological Chemistry 177:2 (1949), 751–766.
18. Guillet, C., Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. The FASEB Journal, 2004 https://doi.org/10.1096/fj.03-1341fje.
19. 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 78:11 (1995), 2336–2344 https://doi.org/10.3168/jds.S0022-0302(95)76860-6.
20. Jin, Y., Yu, Y., Qi, Y., Wang, F., Yan, J., Zou, H., Peptide profiling and the bioactivity character of yogurt in the simulated gastrointestinal digestion. Journal of Proteomics 141 (2016), 24–46 https://doi.org/10.1016/j.jprot.2016.04.010.
21. Katsanos, C.S., Kobayashi, H., Sheffield-Moore, M., Aarsland, A., Wolfe, R.R., A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. American Journal of Physiology. Endocrinology and Metabolism 291:2 (2006), E381–E387 https://doi.org/10.1152/ajpendo.00488.2005.
22. Kim, D.A., Cornec, M., Narsimhan, G., Effect of thermal treatment on interfacial properties of β-lactoglobulin. Journal of Colloid and Interface Science 285:1 (2005), 100–109 https://doi.org/10.1016/j.jcis.2004.10.044.
23. Kim, S.B., Ki, K.S., Khan, M.A., Lee, W.S., Lee, H.J., Ahn, B.S., et al. Peptic and tryptic hydrolysis of native and heated whey protein to reduce its antigenicity. Journal of Dairy Science 90:9 (2007), 4043–4050 https://doi.org/10.3168/jds.2007-0169.
24. Kitabatake, N., Kinekawa, Y.-I., Digestibility of bovine milk whey protein and β-lactoglobulin in vitro and in vivo. Journal of Agricultural and Food Chemistry 46:12 (1998), 4917–4923 https://doi.org/10.1021/jf9710903.
25. Koopman, R., van Loon, L.J.C., Aging, exercise, and muscle protein metabolism. Journal of Applied Physiology 106:6 (2009), 2040–2048 https://doi.org/10.1152/japplphysiol.91551.2008.
26. Kopf-Bolanz, K.A., Schwander, F., Gijs, M., Vergeres, G., Portmann, R., Egger, L., Impact of milk processing on the generation of peptides during digestion. International Dairy Journal 35:2 (2014), 130–138 https://doi.org/10.1016/j.idairyj.2013.10.012.
27. Korhonen, H., Pihlanto-Leppälä, A., Rantamäki, P., Tupasela, T., The functional and biological properties of whey proteins : Prospects for the development of functional foods. 1998 Retrieved from: http://www.doria.fi/handle/10024/15212.
28. Kuznetsova, A., Brockhoff, P.B., Christensen, H.B., lmerTest: tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package), v. 2.0–25. 2014 http://Cran. r-Project. Org/Package= LmerTest.
29. Lambers, T.T., Bosch, W. G. van den, Jong, S. de, Fast and slow Proteins: Modulation of the gastric behavior of whey and casein in vitro. Food Digestion 4:1 (2013), 1–6 https://doi.org/10.1007/s13228-012-0028-7.
30. Le Feunteun, S., Barbé, F., Rémond, D., Ménard, O., Le Gouar, Y., Dupont, D., et al. Impact of the dairy matrix structure on milk protein digestion Kinetics: Mechanistic modelling based on mini-pig in vivo data. Food and Bioprocess Technology 7:4 (2014), 1099–1113 https://doi.org/10.1007/s11947-013-1116-6.
31. Lundin, L., Golding, M., Wooster, T.J., Understanding food structure and function in developing food for appetite control. Nutrition and Dietetics 65 (2008), S79–S85 https://doi.org/10.1111/j.1747-0080.2008.00266.x.
32. Luo, Q., Boom, R.M., Janssen, A.E.M., Digestion of protein and protein gels in simulated gastric environment. Lebensmittel-Wissenschaft und -Technologie- Food Science and Technology 63:1 (2015), 161–168 https://doi.org/10.1016/j.lwt.2015.03.087.
33. Luo, Q., Borst, J.W., Westphal, A.H., Boom, R.M., Janssen, A.E.M., Pepsin diffusivity in whey protein gels and its effect on gastric digestion. Food Hydrocolloids 66 (2017), 318–325 https://doi.org/10.1016/j.foodhyd.2016.11.046.
34. Macierzanka, A., Boettger, F., Lansonneur, L., Groizard, R., Jean, A.-S., Rigby, N.M., Mackie, A.R., The effect of gel structure on the kinetics of simulated gastrointestinal digestion of bovine beta-lactoglobulin. Food Chemistry 134:4 (2012), 2156–2163 https://doi.org/10.1016/j.foodchem.2012.04.018.
35. Mahé, S., Roos, N., Benamouzig, R., Davin, L., Luengo, C., Gagnon, L., et al. Gastrojejunal kinetics and the digestion of [15N]beta-lactoglobulin and casein in humans: The influence of the nature and quantity of the protein. American Journal of Clinical Nutrition 63:4 (1996), 546–552.
36. Mat, D.J.L., Le Feunteun, S., Michon, C., Souchon, I., In vitro digestion of foods using pH-stat and the INFOGEST protocol: Impact of matrix structure on digestion kinetics of macronutrients, proteins and lipids. Food Research International 88:Part B (2016), 226–233 https://doi.org/10.1016/j.foodres.2015.12.002.
37. Minekus, M., Alminger, M., Alvito, P., Ballance, S., Bohn, T., Bourlieu, C., Brodkorb, A., A standardised static in vitro digestion method suitable for food – an international consensus. Food & Function, 5(6), 2014, 1113.
38. Moore, S., Spackman, D.H., Stein, W.H., Chromatography of amino acids on sulfonated polystyrene resins. An improved system. Analytical Chemistry 30:7 (1958), 1185–1190 https://doi.org/10.1021/ac60139a005.
39. Morell, P., Fiszman, S., Llorca, E., Hernando, I., Designing added-protein yogurts: Relationship between in vitro digestion behavior and structure. Food Hydrocolloids 72 (2017), 27–34 https://doi.org/10.1016/j.foodhyd.2017.05.026.
40. Nguyen, T.T.P., Bhandari, B., Cichero, J., Prakash, S., Gastrointestinal digestion of dairy and soy proteins in infant formulas: An in vitro study. Food Research International 76 (2015), 348–358 https://doi.org/10.1016/j.foodres.2015.07.030.
41. Nicolai, T., Britten, M., Schmitt, C., β-Lactoglobulin and WPI aggregates: Formation, structure and applications. Food Hydrocolloids 25:8 (2011), 1945–1962 https://doi.org/10.1016/j.foodhyd.2011.02.006.
42. O'Loughlin, I.B., Murray, B.A., Kelly, P.M., FitzGerald, R.J., Brodkorb, A., Enzymatic hydrolysis of heat-induced aggregates of whey protein isolate. Journal of Agricultural and Food Chemistry 60:19 (2012), 4895–4904 https://doi.org/10.1021/jf205213n.
43. Pennings, B., Boirie, Y., Senden, J.M.G., Gijsen, A.P., Kuipers, H., van Loon, L.J.C., Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. American Journal of Clinical Nutrition 93:5 (2011), 997–1005 https://doi.org/10.3945/ajcn.110.008102.
44. Peram, M.R., Loveday, S.M., Ye, A., Singh, H., In vitro gastric digestion of heat-induced aggregates of β-lactoglobulin. Journal of Dairy Science 96:1 (2013), 63–74 https://doi.org/10.3168/jds.2012-5896.
45. Reddy, I.M., Kella, N.K.D., Kinsella, J.E., Structural and conformational basis of the resistance of.beta.-lactoglobulin to peptic and chymotryptic digestion. Journal of Agricultural and Food Chemistry 36:4 (1988), 737–741 https://doi.org/10.1021/jf00082a015.
46. Rieu, I., Balage, M., Sornet, C., Giraudet, C., Pujos, E., Grizard, J., Dardevet, D., Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidaemia: Leucine and protein metabolism in the elderly. The Journal of Physiology 575:1 (2006), 305–315 https://doi.org/10.1113/jphysiol.2006.110742.
47. Rinaldi, L., Gauthier, S.F., Britten, M., Turgeon, S.L., In vitro gastrointestinal digestion of liquid and semi-liquid dairy matrixes. Lebensmittel-Wissenschaft und -Technologie- Food Science and Technology 57:1 (2014), 99–105 https://doi.org/10.1016/j.lwt.2014.01.026.
48. Rinaldi, L., Rioux, L.-E., Britten, M., Turgeon, S.L., In vitro bioaccessibility of peptides and amino acids from yogurt made with starch, pectin, or β-glucan. International Dairy Journal 46:Supplement C (2015), 39–45 https://doi.org/10.1016/j.idairyj.2014.09.005.
49. Shani-Levi, C., Alvito, P., Andrés, A., Assunção, R., Barberá, R., Blanquet-Diot, S., Lesmes, U., Extending in vitro digestion models to specific human populations: Perspectives, practical tools and bio-relevant information. Special Issues from the 29th EFFoST International Conference 60:Supplement C (2017), 52–63 https://doi.org/10.1016/j.tifs.2016.10.017.
50. Singh, T.K., Øiseth, S.K., Lundin, L., Day, L., Influence of heat and shear induced protein aggregation on the in vitro digestion rate of whey proteins. Food Function 5:11 (2014), 2686–2698 https://doi.org/10.1039/C4FO00454J.
51. Singh, H., Ye, A., Ferrua, M.J., Aspects of food structures in the digestive tract. Current Opinion in Food Science 3:Supplement C (2015), 85–93 https://doi.org/10.1016/j.cofs.2015.06.007.
52. Takagi, K., Teshima, R., Okunuki, H., Sawada, J., Comparative study of in vitro digestibility of food proteins and effect of preheating on the digestion. Biological and Pharmaceutical Bulletin 26:7 (2003), 969–973 https://doi.org/10.1248/bpb.26.969.
53. Tang, J.E., Moore, D.R., Kujbida, G.W., Tarnopolsky, M.A., Phillips, S.M., Ingestion of whey hydrolysate, casein, or soy protein isolate: Effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. Journal of Applied Physiology (Bethesda, Md.: 1985) 107:3 (2009), 987–992 https://doi.org/10.1152/japplphysiol.00076.2009.
54. Thévenot, J., Cauty, C., Legland, D., Dupont, D., Floury, J., Pepsin diffusion in dairy gels depends on casein concentration and microstructure. Food Chemistry 223 (2017), 54–61 https://doi.org/10.1016/j.foodchem.2016.12.014.
55. Tunick, M.H., Ren, D.X., Van Hekken, D.L., Bonnaillie, L., Paul, M., Kwoczak, R., et al. Effect of heat and homogenization on in vitro digestion of milk. Journal of Dairy Science 99:6 (2016), 4124–4139 https://doi.org/10.3168/jds.2015-10474.
56. Volpi, E., Kobayashi, H., Sheffield-Moore, M., Mittendorfer, B., Wolfe, R.R., Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. American Journal of Clinical Nutrition 78:2 (2003), 250–258.