The effect of milk proteins on the bioaccessibility of green tea flavan-3-ols

Food Research International

Volumn 66, Issue , 2014, Pages 297-305

  Moser, Sydney ^a   Chegeni, Mohammad ^a   Jones, Owen G ^a   Liceaga, Andrea ^a   Ferruzzi, Mario G ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Bioaccessibility; Flavan 3 ol; Fluorometry; Green tea; Milk Protein; SDS PAGE

Indexed keywords

BIOACCESSIBILITY; FLAVAN-3-OLS; FLUOROMETRY; GREEN TEA; MILK PROTEIN; SDS-PAGE;

EID: 84908296246     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2014.09.018     Document Type: Article

References (76)

1. Al-Numair K.S., Ahmed S.E.B., Al-Assaf A.H., Alamri M.S. Hydrochloric acid extractable minerals and phytate and polyphenols contents of sprouted faba and white bean cultivars. Food Chemistry 2009, 113(4):997-1002.
2. Anema S.G., McKenna A.B. Reaction kinetics of thermal denaturation of whey proteins in heated reconstituted whole milk. Journal of Agricultural and Food Chemistry 1996, 44(2):422-428.
3. Augustin M. Mineral salts and their effect on milk functionality. Proceedings Dairy Ingredient Science 2000, Melbourne, Australia, 28-30 July, 2000 2000, Vol. 55:61-64.
4. Bohin M.C., Vincken J.-P., van der Hijden H.T.W.M., Gruppen H. Efficacy of food proteins as carriers for flavonoids. Journal of Agricultural and Food Chemistry 2012, 60(16):4136-4143.
5. Bonner M.R., Rothman N., Mumford J.L., He X., Shen M., Welch R., et al. Green tea consumption, genetic susceptibility, PAH-rich smoky coal, and the risk of lung cancer. Mutation Research 2005, 582(1-2):53-60.
6. Chandronitha C., Ananthi S., Ramakrishnan G., Lakshmisundaram R., Gayathri V., Vasanthi H.R. Protective role of tannin-rich fraction of Camellia sinensis in tissue arsenic burden in Sprague-Dawley rats. Human & Experimental Toxicology 2010, 29(9):705-719.
7. Changani S., Belmar-Beiny M., Fryer P. Engineering and chemical factors associated with fouling and cleaning in milk processing. Experimental Thermal and Fluid Science 1997, 14(4):392-406.
8. Chun O.K., Chung S.J., Song W.O. Estimated dietary flavonoid intake and major food sources of US adults. Journal of Nutrition 2007, 137(5):1244-1252.
9. Devine A., Hodgson J.M., Dick I.M., Prince R.L. Tea drinking is associated with benefits on bone density in older women. The American Journal of Clinical Nutrition 2007, 86(4):1243-1247.
10. Ferruzzi M.G., Green R.J. Analysis of catechins from milk-tea beverages by enzyme assisted extraction followed by high performance liquid chromatography. Food Chemistry 2006, 99(3):484-491.
11. Gaucheron F. The minerals of milk. Reproduction, Nutrition, Development 2005, 45(4):473-484.
12. Gravel P. Two-dimensional polyacrylamide gel electrophoresis of proteins using carrier ampholyte pH gradients in the first dimension. The protein protocols handbook 2002, 187-191. Humana Press Inc., New Jersey. 3rd ed. J.M. Walker (Ed.).
13. Green R.J., Murphy A.S., Schulz B., Watkins B.A., Ferruzzi M.G. Common tea formulations modulate in vitro digestive recovery of green tea catechins. Molecular Nutrition & Food Research 2007, 51(9):1152-1162.
14. Grove K.A., Sae-Tan S., Kennett M.J., Lambert J.D. (-)-Epigallocatechin-3-gallate inhibits pancreatic lipase and reduces body weight gain in high fat-fed obese mice. Obesity 2012, 20(11):2311-2313.
15. Hasni I., Bourassa P., Hamdani S., Samson G., Carpentier R., Tajmir-Riahi H.A. Interaction of milk alpha- and beta-caseins with tea polyphenols. Food Chemistry 2011, 126(2):630-639.
16. He Q., Yuanping L., Yao K. Effects of tea polyphenols on the activities of alpha-amylase, pepsin, trypsin, and lipase. Food Chemistry 2006, 101:1178-1182.
17. Hertog M.G., Sweetnam P.M., Fehily A.M., Elwood P.C., Kromhout D. Antioxidant flavonols and ischemic heart disease in a Welsh population of men: the Caerphilly Study. American Journal of Clinical Nutrition 1997, 65(5):1489-1494.
18. Hooper L., Kroon P.A., Rimm E.B., Cohn J.S., Harvey I., Le Cornu K.A., et al. Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials. American Journal of Clinical Nutrition 2008, 88(1):38-50.
19. Hu G., Bidel S., Jousilahti P., Antikainen R., Tuomilehto J. Coffee and tea consumption and the risk of Parkinson's disease. Movement Disorders 2007, 22(15):2242-2248.
20. Jenness R., Koops J. Preparation and properties of a salt solution which simulates milk ultrafiltrate. Netherlands Institute for Dairy Research 1962, 16:153-164.
21. Jöbstl E., Fairclough J.P.A., Davies A.P., Williamson M.P. Creaming in black tea. Journal of Agricultural and Food Chemistry 2005, 53(20):7997-8002.
22. Kanakis C.D., Hasni I., Bourassa P., Tarantilis P.A., Polissiou M.G., Tajmir-Riahi H.A. Milk beta-lactoglobulin complexes with tea polyphenols. Food Chemistry 2011, 127(3):1046-1055.
23. Kean E.G., Bordenave N., Ejeta G., Hamaker B.R., Ferruzzi M.G. Carotenoid bioaccessibility from whole grain and decorticated yellow endosperm sorghum porridge. Journal of Cereal Science 2011, 54(3):450-459.
24. Kelly P., O'Keeffe A., Keogh M., Phelan J. Studies of milk composition and its relationship to some processing criteria: III: Seasonal variation in heat stability of milk. Irish Journal of Food Science and Technology 1982, 29-38.
25. Keogh J.B., McInerney J., Clifton P.M. The effect of milk protein on the bioavailability of cocoa polyphenols. Journal of Food Science 2007, 72(3):S230-S233.
26. Kostyuk V.A., Potapovich A.I., Strigunova E.N., Kostyuk T.V., Afanas'ev I.B. Experimental evidence that flavonoid metal complexes may act as mimics of superoxide dismutase. Archives of biochemistry and biophysics 2004, 428(2):204-208.
27. Kyle J.A.M., Morrice P.C., McNeill G., Duthie G.G. Effects of infusion time and addition of milk on content and absorption of polyphenols from black tea. Journal of Agricultural and Food Chemistry 2007, 55:4889-4894.
28. Lee K.W., Kang N.J., Oak M.H., Hwang M.K., Kim J.H., Schini-Kerth V.B., et al. Cocoa procyanidins inhibit expression and activation of MMP-2 in vascular smooth muscle cells by direct inhibition of MEK and MT1-MMP activities. Cardiovascular Research 2008, 79(1):34-41.
29. Li Y., Cao Z., Zhu H. Upregulation of endogenous antioxidants and phase 2 enzymes by the red wine polyphenol, resveratrol in cultured aortic smooth muscle cells leads to cytoprotection against oxidative and electrophilic stress. Pharmacological Research 2006, 53(1):6-15.
30. Lönnerdal B., Yuen M., Huang S. Calcium, iron, zinc, copper and manganese bioavailability from infant formulas and weaning diets assessed in rat pups. Nutrition Research 1994, 14(10):1535-1548.
31. Lorenz M., Jochmann N., von Krosigk A., Martus P., Baumann G., Stangl K., et al. Addition of milk prevents vascular protective effects of tea. European Heart Journal 2007, 28(2):219-223.
32. Lorenz M., Stangl K., Stangl V. Vascular effects of tea are suppressed by soy milk. Atherosclerosis 2009, 206(1):31-32.
33. Mandalari G., Adel-Patient K., Barkholt V., Baro C., Bennett L., Bublin M., et al. In vitro digestibility of β-casein and β-lactoglobulin under simulated human gastric and duodenal conditions: A multi-laboratory evaluation. Regulatory Toxicology and Pharmacology 2009, 55(3):372-381.
34. McMahon D.J., Oommen B. Supramolecular structure of the casein micelle. Journal of Dairy Science 2008, 91(5):1709-1721.
35. Mouécoucou J., Villaume C., Sanchez C., Méjean L. β-Lactoglobulin/polysaccharide interactions during in vitro gastric and pancreatic hydrolysis assessed in dialysis bags of different molecular weight cut-offs. Biochimica et Biophysica Acta (BBA) - General Subjects 2004, 1670(2):105-112.
36. Naz N., Siddiqi R., Dew T.P., Williamson G. Epigallocatechin-3-gallate inhibits lactase but is alleviated by salivary proline-rich proteins. Journal of Agricultural and Food Chemistry 2011, 59(6):2734-2738.
37. Neilson A.P., George J.C., Janle E.M., Mattes R.D., Rudolph R., Matusheski N.V., et al. Influence of chocolate matrix composition on cocoa flavan-3-ol bioaccessibility in vitro and bioavailability in humans. Journal of Agricultural and Food Chemistry 2009, 57(20):9418-9426.
38. Neilson A.P., Hopf A.S., Cooper B.R., Pereira M.A., Bomser J.A., Ferruzzi M.G. Catechin degradation with concurrent formation of homo- and heterocatechin dimers during in vitro digestion. Journal of Agricultural and Food Chemistry 2007, 55(22):8941-8949.
39. Ng T.P., Feng L., Niti M., Kua E.H., Yap K.B. Tea consumption and cognitive impairment and decline in older Chinese adults. American Journal of Clinical Nutrition 2008, 88(1):224-231.
40. Ohno M., Sakamoto K.Q., Ishizuka M., Fujita S. Crude cacao Theobroma cacao extract reduces mutagenicity induced by benzo[a]pyrene through inhibition of CYP1A activity in vitro. Phytotherapy Research 2009, 23(8):1134-1139.
41. Otte J., Zakora M., Qvist K.B., Olsen C.E., Barkholt V. Hydrolysis of bovine β-lactoglobulin by various proteases and identification of selected peptides. International Dairy Journal 1997, 7(12):835-848.
42. Petermann A., Miene C., Schultz-Raffelt G., Palige K., Glei M., Bohmer F.D. GSTT2, a phase II gene induced by apple polyphenols, protects colon epithelial cells against genotoxic damage. Molecular Nutrition & Food Research 2009, 53(10):1245-1253.
43. Peters C.M., Green R.J., Janle E.M., Ferruzzi M.G. Formulation with ascorbic acid and sucrose modulates catechin bioavailability from green tea. Food Research International 2010, 43(1):95-102.
44. Reddy V.C., Sagar G.V.V., Sreeramulu D., Venu L., Raghunath M. Addition of milk does not alter the antioxidant activity of black tea. Annals of Nutrition and Metabolism 2005, 49(3):189-195.
45. Renouf M., Marmet C., Guy P., Fraering A.-L., Longet K., Moulin J., et al. Nondairy creamer, but not milk, delays the appearance of coffee phenolic acid equivalents in human plasma. The Journal of Nutrition 2010, 140(2):259-263.
46. Riehle P., Vollmer M., Rohn S. Phenolic compounds in Cistus incanus herbal infusions-Antioxidant capacity and thermal stability during the brewing process. Food Research International 2012, 53(2):891-899.
47. Roberts E. The phenolic substances of manufactured tea. X.-The creaming down of tea liquors. Journal of the Science of Food and Agriculture 1963, 14(10):700-705.
48. Roura E., Andres-Lacueva C., Estruch R., Mata-Bilbao M.L., Izquierdo-Pulido M., Waterhouse A.L., et al. Milk does not affect the bioavailability of cocoa powder flavonoid in healthy human. Annals of Nutrition and Metabolism 2007, 51(6):493-498.
49. Sanyal A.J., Hirsch J.I., Moore E.W. High-affinity binding is essential for enhancement of intestinal Fe2+ and Ca2+ uptake by bile salts. Gastroenterology 1992, 102(6):1997-2005.
50. Serafini M., Bugianesi R., Maiani G., Valtuena S., De Santis S., Crozier A. Plasma antioxidants from chocolate. Nature 2003, 424(6952):1013.
51. Serafini M., Testa M.F., Villano D., Pecorari M., Peluso I., Brambilla A., et al. Antioxidant activity of blueberry fruit is impaired by the association with milk. Annals of Nutrition and Metabolism 2009, 55:161.
52. Sherwin C.P., Foegeding E.A. The effect of CaCl2 on aggregation of whey proteins. Milchwissenschaft 1997, 52(2):93-96.
53. Soares S., Mateus N., Freitas V. Interaction of different polyphenols with bovine serum albumin (BSA) and human salivary alpha-amylase (HSA) by fluorescence quenching. Journal of Agricultural and Food Chemistry 2007, 55(16):6726-6735.
54. Song W.O., Chun O.K. Tea is the major source of flavan-3-ol and flavonol in the U.S. diet. The Journal of Nutrition 2008, 138(8):1543S-1547S.
55. Song Y., Manson J.E., Buring J.E., Sesso H.D., Liu S. Associations of dietary flavonoids with risk of type 2 diabetes, and markers of insulin resistance and systemic inflammation in women: A prospective study and cross-sectional analysis. Journal of the American College of Nutrition 2005, 24(5):376-384.
56. Song, et al. Thermal degradation of green tea flavan-3-ols and the formation of hetero- and homo-catechin dimers in model dairy beverages. Food Chemistry 2014, (in review).
57. Tagliazucchi D.V., Verzelloni E., Conte A. Effect of some phenolic compounds and beverages on pepsin activity during stimulated gastric digestion. Journal of Agricultural and Food Chemistry 2005, 53(22):8706-8713.
58. Tantoush Z., Apostolovic D., Kravic B., Prodic I., Mihajlovic L., Stanic-Vucinic D., et al. Green tea catechins of food supplements facilitate pepsin digestion of major food allergens, but hampers their digestion if oxidized by phenol oxidase. Journal of Functional Foods 2012, 4(3):650-660.
59. Thakkar S.K., Maziya-Dixon B., Dixon A.G.O., Failla M.L. beta-Carotene micellarization during in vitro digestion and uptake by Caco-2 cells is directly proportional to beta-carotene content in different genotypes of cassava. Journal of Nutrition 2007, 137(10):2229-2233.
60. U.S.Department of Agriculture, Agricultural Research Service USDA Database for the Flavonoid Content of Selected Foods 2011, Release 3.0. Nutrient Data Laboratory Home Page: http://www.ars.usda.gov/nutrientdata/flav.
61. Unno T., Osada C., Motoo Y., Suzuki Y., Kobayashi M., Nozawa A. Dietary tea catechins increase fecal energy in rats. Journal of Nutritional Science and Vitaminology 2009, 55(5):447-451.
62. van der Burg-Koorevaar M.C., Miret S., Duchateau G.S. Effect of milk and brewing method on black tea catechin bioaccessibility. Journal of Agricultural and Food Chemistry 2011, 59(14):7752-7758.
63. van Dieren S., Uiterwaal C.S.P.M., van der Schouw Y.T., van der A D.L., Boer J.M.A., Spijkerman A., Grobbee D.E., Beulens J.W.J. Coffee and tea consumption and risk of type 2 diabetes. Diabetologia 2009, 52(12):2561-2569.
64. van het Hof K.H., Kivits G.A., Weststrate J.A., Tijburg L.B. Bioavailability of catechins from tea: the effect of milk. European Journal of Clinical Nutrition 1998, 52(5):356-359.
65. Vegarud G.E., Langsrud T., Svenning C. Mineral-binding milk proteins and peptides; occurrence, biochemical and technological characteristics. British Journal of Nutrition 2000, 84:S91-S98.
66. Vitali D., Dragojevic I.V., Sebecic B. Bioaccessibility of Ca, Mg, Mn and Cu from whole grain tea-biscuits: Impact of proteins, phytic acid and polyphenols. Food Chemistry 2008, 110(1):62-68.
67. von Staszewski M., Jara F.L., Ruiz A.L.T.G., Jagus R.J., Carvalho J.E., Pilosof A.M.R. Nanocomplex formation between β-lactoglobulin or caseinomacropeptide and green tea polyphenols: Impact on protein gelation and polyphenols antiproliferative activity. Journal of Functional Foods 2012, 4(4):800-809.
68. Wang Y., Chung S.J., Song W.O., Chun O.K. Estimation of daily proanthocyanidin intake and major food sources in the U.S. diet. Journal of Nutrition 2011, 141(3):447-452.
69. Weisburger J.H. Tea and health: A historical perspective. Cancer Letters 1997, 114(1-2):315-317.
70. Xie Y., Kosinska A., Xu H., Andlauer W. Milk enhances intestinal absorption of green tea catechins in in vitro digestion/Caco-2 cells model. Food Research International 2014, 53(2):793-800.
71. Yamada K., Abe T., Tanizawa Y. Black tea stain formed on the surface of teacups and pots. Part 2 - Study of the structure change caused by aging and calcium addition. Food Chemistry 2007, 103(1):8-14.
72. Yang C.S., Landau J.M. Effects of tea consumption on nutrition and health. The Journal of Nutrition 2000, 130(10):2409-2412.
73. Yaşar S.B., Güçer Ş. Fractionation analysis of magnesium in olive products by atomic absorption spectrometry. Analytica Chimica Acta 2004, 505(1):43-49.
74. Yuan J.M., Gao Y.T., Yang C.S., Yu M.C. Urinary biomarkers of tea polyphenols and risk of colorectal cancer in the Shanghai Cohort Study. International Journal of Cancer 2007, 120(6):1344-1350.
75. Yuan J.H., Li Y.Q., Yang X.Y. Inhibition of epigallocatechin gallate on orthotopic colon cancer by upregulating the Nrf2-UGT1A signal pathway in nude mice. Pharmacology 2007, 80(4):269-278.
76. Zuchi C., Ambrosio G., Luscher T.F., Landmesser U. Nutraceuticals in cardiovascular prevention: Lessons from studies on endothelial function. Cardiovascular Therapeutics 2010, 28(4):187-201.