Whey protein isolate counteracts the effects of a high-fat diet on energy intake and hypothalamic and adipose tissue expression of energy balance-related genes

British Journal of Nutrition

Volumn 110, Issue 11, 2013, Pages 2114-2126

  Mcallan, Liam ^a,b   Keane, Deirdre ^c   Schellekens, Harriët ^b   Roche, Helen M ^c   Korpela, Riitta ^d   Cryan, John F ^b,e   Nilaweera, Kanishka N ^a  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Energy balance; Gene expression; Mice; Obesity; Whey proteins

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA; MILK PROTEIN; PROTEIN TAG;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CALORIC INTAKE; CPT1B GENE; DIET SUPPLEMENTATION; ENERGY BALANCE; ENERGY EXPENDITURE; FAT MASS; GENE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUT4 GENE; HORMONE BLOOD LEVEL; HYPOTHALAMUS; INFLAMMATION; INSR GENE; INSULIN BLOOD LEVEL; LIPID DIET; LIPID METABOLISM; LOCOMOTION; MALE; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN INTAKE; SIGNAL TRANSDUCTION; THERMOGENESIS;

ADIPOSE TISSUE, WHITE; ADIPOSITY; ANIMALS; BEHAVIOR, ANIMAL; CARNITINE O-PALMITOYLTRANSFERASE; DIET, HIGH-FAT; DISEASE SUSCEPTIBILITY; ENERGY INTAKE; EPIDIDYMIS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORTER TYPE 4; HYPOTHALAMUS; MALE; MICE; MICE, INBRED C57BL; MILK PROTEINS; OVERWEIGHT; RECEPTOR, INSULIN; RECEPTORS, LEPTIN;

EID: 84888326033     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114513001396     Document Type: Article

References (74)

1. Bruce KD & Byrne CD (2009) The metabolic syndrome:common origins of a multifactorial disorder. Postgrad Med J 85, 614-621
2. Caterson ID, Hubbard V, Bray GA, et al. (2004) Prevention Conference VII. Obesity, a worldwide epidemic related to heart disease and stroke: Group III: Worldwide comorbidities of obesity. Circulation 110, e476-e483
3. Chalkley SM, Hettiarachchi M, Chisholm DJ, et al. (2002) Long-term high-fat feeding leads to severe insulin resistance but not diabetes in Wistar rats. Am J Physiol Endocrinol Metab 282, E1231-E1238
4. Hill JO & Peters JC (2002) Biomarkers and functional foods for obesity and diabetes. Br J Nutr 88, S213-S218
5. Lin S, Thomas TC, Storlien LH, et al. (2000) Development of high fat diet-induced obesity and leptin resistance in C57Bl/6J mice. Int J Obes Relat Metab Disord 24, 639-646
6. Krissansen GW (2007) Emerging health properties of whey proteins and their clinical implications. J Am Coll Nutr 26,713S-723S.
7. Acheson KJ, Blondel-Lubrano A, Oguey-Araymon S, et al. (2011) Protein choices targeting thermogenesis and metabolism. Am J Clin Nutr 93, 525-534
8. Gunnarsson PT, Winzell MS, Deacon CF, et al. (2006) Glucose-induced incretin hormone release and inactivation are differently modulated by oral fat and protein in mice. Endocrinology 147, 3173-3180
9. Nilsson M, Holst JJ & Bjorck IM (2007) Metabolic effects of amino acid mixtures and whey protein in healthy subjects:studies using glucose-equivalent drinks. Am J Clin Nutr 85,996-1004
10. Shertzer HG, Woods SE, Krishan M, et al. (2011) Dietary whey protein lowers the risk for metabolic disease in mice fed a high-fat diet. J Nutr 141, 582-587
11. Hall WL, Millward DJ, Long SJ, et al. (2003) Casein and whey exert different effects on plasma amino acid profiles,gastrointestinal hormone secretion and appetite. Br J Nutr 89, 239-248
12. Zhou J, Keenan MJ, Losso JN, et al. (2011) Dietary whey protein decreases food intake and body fat in rats. Obesity 19, 1568-1573
13. Yu Y, South T, Huang XF (2009) Inter-meal interval is increased in mice fed a high whey, as opposed to soy and gluten, protein diets. Appetite 52, 372-379
14. Benton MJ & Swan PD (2007) Effect of protein ingestion on energy expenditure and substrate utilization after exercise in middle-aged women. Int J Sport Nutr Exerc Metab 17,544-555
15. Pichon L, Potier M, Tome D, et al. (2008) High-protein diets containing different milk protein fractions differently influence energy intake and adiposity in the rat. Br J Nutr 739-748
16. Royle PJ, McIntosh GH & Clifton PM (2008) Whey protein isolate and glycomacropeptide decrease weight gain and alter body composition in male Wistar rats. Br J Nutr 100,88-93
17. Veldhorst MA, Nieuwenhuizen AG, Hochstenbach-Waelen A,et al. (2009) Dose-dependent satiating effect of whey relative to casein or soy. Physiol Behav 96, 675-682
18. Luhovyy BL, Akhavan T & Anderson GH (2007) Whey proteins in the regulation of food intake and satiety. J Am Coll Nutr 26, 704S-712S.
19. McAllan L, Cotter PD, Roche HM, et al. (2012) Bioactivity in whey proteins influencing energy balance. J Metab Synd 1, 107
20. Pilvi TK, Harala S, Korpela R, et al. (2009) Effects of highcalcium diets with different whey proteins on weight loss and weight regain in high-fat-fed C57BL/6J mice. Br J Nutr 102, 337-341
21. Pilvi TK, Korpela R, Huttunen M, et al. (2007) High-calcium diet with whey protein attenuates body-weight gain in highfat- fed C57Bl/6J mice. Br J Nutr 98, 900-907
22. Shi J, Tauriainen E, Martonen E, et al. (2011) Whey protein isolate protects against diet-induced obesity and fatty liver formation. Int Dairy J 21, 513-522
23. Shi J, Ahlroos-Lehmus A, Pilvi TK, et al. (2012) Metabolic effects of a novel microfiltered native whey protein in diet-induced obese mice. J Funct Foods 4, 440-449
24. Weir JB (1949) New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 109, 1-9
25. Longo KA, Charoenthongtrakul S, Giuliana DJ, et al. (2010) The 24-hour respiratory quotient predicts energy intake and changes in body mass. Am J Physiol Regul Integr Comp Physiol 298, R747-R754
26. Matthews DR, Hosker JP, Rudenski AS, et al. (1985) Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412-419
27. Folch J, Lees M & Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497-509
28. Guo H, Xia M, Zou T, et al. (2012) Cyanidin 3-glucoside attenuates obesity-associated insulin resistance and hepatic steatosis in high-fat diet-fed and db/db mice via the transcription factor FoxO1. J Nutr Biochem 23, 349-360
29. Hoggard N, Cruickshank M, Moar KM, et al. (2009) Inhibin betaB expression in murine adipose tissue and its regulation by leptin, insulin and dexamethasone. J Mol Endocrinol 43,171-177
30. Mracek T, Gao D, Tzanavari T, et al. (2010) Downregulation of zinc-{alpha}2-glycoprotein in adipose tissue and liver of obese ob/ob mice and by tumour necrosis factor-alpha in adipocytes. J Endocrinol 204, 165-172
31. Yasmeen R, Reichert B, Deiuliis J, et al. (2013) Autocrine function of aldehyde dehydrogenase 1 as a determinant of diet- and sex-specific differences in visceral adiposity. Diabetes 62, 124-136
32. Giraudo SQ, Della-Fera MA, Proctor L, et al. (2010) Maternal high fat feeding and gestational dietary restriction: Effects on offspring body weight, food intake and hypothalamic gene expression over three generations in mice. Pharmacol Biochem Behav 97, 121-129
33. Hao L, Li M, Dai J, et al. (2010) Reduced somatostatin in hypothalamus of young male mouse increases local but not circulatory GH. Neurochem Res 35, 143-151
34. Sellayah D, Sek K, Anthony FW, et al. (2008) Sensitivity of housekeeping genes in the hypothalamus to mismatch in diets between pre- and postnatal periods in mice. Neurosci Lett 447, 54-57
35. Czyzyk TA, Nogueiras R, Lockwood JF, et al. (2010) kappa-Opioid receptors control the metabolic response to a high-energy diet in mice. FASEB J 24, 1151-1159
36. Dubois SK, Kishimoto I, Lillis TO, et al. (2000) A genetic model defines the importance of the atrial natriuretic peptide receptor (guanylyl cyclase-A) in the regulation of kidney function. Proc Natl Acad Sci U S A 97, 4369-4373
37. Nogueiras R, Lopez M & Dieguez C (2010) Regulation of lipid metabolism by energy availability: A role for the central nervous system. Obes Rev 11, 185-201
38. Nogueiras R, Wiedmer P, Perez-Tilve D, et al. (2007) The central melanocortin system directly controls peripheral lipid metabolism. J Clin Invest 117, 3475-3488
39. Ryan KK, Woods SC & Seeley RJ (2012) Central nervous system mechanisms linking the consumption of palatable high-fat diets to the defense of greater adiposity. Cell Metab 15, 137-149
40. Saegusa Y, Takeda H, Muto S, et al. (2011) Decreased plasma ghrelin contributes to anorexia following novelty stress. Am J Physiol Endocrinol Metab 301, E685-E696
41. Westerterp KR (1993) Food quotient, respiratory quotient,and energy balance. Am J Clin Nutr 57, 759S-764S (discussion 764S-765S
42. Hanson BA & Lester RL (1980) The extraction of inositolcontaining phospholipids and phosphatidylcholine from Saccharomyces cerevisiae and Neurospora crassa. J Lipid Res 21, 309-315
43. Herman MA, Peroni OD, Villoria J, et al. (2012) A novel ChREBP isoform in adipose tissue regulates systemic glucose metabolism. Nature 484, 333-338
44. Kersten S (2001) Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Rep 2, 282-286
45. Collins S, Daniel KW, Petro AE, et al. (1997) Strain-specific response to beta 3-adrenergic receptor agonist treatment of diet-induced obesity in mice. Endocrinology 138, 405-413
46. Moraes RC, Blondet A, Birkenkamp-Demtroeder K, et al. (2003) Study of the alteration of gene expression in adipose tissue of diet-induced obese mice by microarray and reverse transcription-polymerase chain reaction analyses. Endocrinology 144, 4773-4782
47. Sawa M & Harada H (2006) Recent developments in the design of orally bioavailable beta3-adrenergic receptor agonists. Curr Med Chem 13, 25-37
48. Ryan KK, Li B, Grayson BE, et al. (2011) A role for central nervous system PPAR-gamma in the regulation of energy balance. Nat Med 17, 623-626
49. Diano S, Liu ZW, Jeong JK, et al. (2011) Peroxisome proliferation- associated control of reactive oxygen species sets melanocortin tone and feeding in diet-induced obesity. Nat Med 17, 1121-1127
50. Bonnefont JP, Djouadi F, Prip-Buus C, et al. (2004) Carnitine palmitoyltransferases 1 and 2: Biochemical, molecular and medical aspects. Mol Aspects Med 25, 495-520
51. Gao XF, Chen W, Kong XP, et al. (2009) Enhanced susceptibility of Cpt1c knockout mice to glucose intolerance induced by a high-fat diet involves elevated hepatic gluconeogenesis and decreased skeletal muscle glucose uptake. Diabetologia 52, 912-920
52. Borg ML, Omran SF, Weir J, et al. (2012) Consumption of a high-fat diet, but not regular endurance exercise training,regulates hypothalamic lipid accumulation in mice. J Physiol 590, 4377-4389
53. Posey KA, Clegg DJ, Printz RL, et al. (2009) Hypothalamic proinflammatory lipid accumulation, inflammation,and insulin resistance in rats fed a high-fat diet. Am J Physiol Endocrinol Metab 296, E1003-E1012
54. Morifuji M, Sakai K, Sanbongi C, et al. (2005) Dietary whey protein downregulates fatty acid synthesis in the liver, but upregulates it in skeletal muscle of exercise-trained rats. Nutrition 21, 1052-1058
55. Fielding BA & Frayn KN (1998) Lipoprotein lipase and the disposition of dietary fatty acids. Br J Nutr 80, 495-502
56. Gimeno RE (2007) Fatty acid transport proteins. Curr Opin Lipidol 18, 271-276
57. Pilvi TK, Storvik M, Louhelainen M, et al. (2008) Effect of dietary calcium and dairy proteins on the adipose tissue gene expression profile in diet-induced obesity. J Nutrigenet Nutrigenomics 1, 240-251
58. McAllan L, Cotter PD, Roche HM, et al. (2013) Impact of leucine on energy balance. J Physiol Biochem 69, 155-163
59. Nogueiras R, Perez-Tilve D, Veyrat-Durebex C, et al. (2009) Direct control of peripheral lipid deposition by CNS GLP-1 receptor signaling is mediated by the sympathetic nervous system and blunted in diet-induced obesity. J Neurosci 29,5916-5925
60. Gustafson B, Gogg S, Hedjazifar S, et al. (2009) Inflammation and impaired adipogenesis in hypertrophic obesity in man. Am J Physiol Endocrinol Metab 297, E999-E1003
61. Isakson P, Hammarstedt A, Gustafson B, et al. (2009) Impaired preadipocyte differentiation in human abdominal obesity: Role of Wnt, tumor necrosis factor-alpha, and inflammation. Diabetes 58, 1550-1557
62. Harford KA, Reynolds CM, McGillicuddy FC, et al. (2011) Fats, inflammation and insulin resistance: Insights to the role of macrophage and T-cell accumulation in adipose tissue. Proc Nutr Soc 70, 408-417
63. Lin S, Storlien LH & Huang XF (2000) Leptin receptor, NPY,POMC mRNA expression in the diet-induced obese mouse brain. Brain Res 875, 89-95
64. Munzberg H & Myers MG Jr (2005) Molecular and anatomical determinants of central leptin resistance. Nat Neurosci 8,566-570
65. Van Heek M, Compton DS, France CF, et al. (1997) Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J Clin Invest 99, 385-390
66. Levin BE & Dunn-Meynell AA (2002) Reduced central leptin sensitivity in rats with diet-induced obesity. Am J Physiol Regul Integr Comp Physiol 283, R941-R948
67. Felig P (1984) Insulin is the mediator of feeding-related thermogenesis: Insulin resistance and/or deficiency results in a thermogenic defect which contributes to the pathogenesis of obesity. Clin Physiol 4, 267-273
68. Kahn BB & Flier JS (2000) Obesity and insulin resistance. J Clin Invest 106, 473-481
69. Pedersen O, Kahn CR, Flier JS, et al. (1991) High fat feeding causes insulin resistance and a marked decrease in the expression of glucose transporters (Glut 4) in fat cells of rats. Endocrinology 129, 771-777
70. De Souza CT, Araujo EP, Bordin S, et al. (2005) Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 146, 4192-4199
71. McGillicuddy FC, Harford KA, Reynolds CM, et al. (2011) Lack of interleukin-1 receptor I (IL-1RI) protects mice from high-fat diet-induced adipose tissue inflammation coincident with improved glucose homeostasis. Diabetes 60, 1688-1698
72. Townsend KL, Lorenzi MM & Widmaier EP (2008) High-fat diet-induced changes in body mass and hypothalamic gene expression in wild-type and leptin-deficient mice. Endocrine 33, 176-188
73. Nilaweera KN, Ozanne D, Wilson D, et al. (2007) G proteincoupled receptor 101 mRNA expression in the mouse brain:altered expression in the posterior hypothalamus and amygdala by energetic challenges. J Neuroendocrinol 19, 34-45
74. Lu M, Sarruf DA, Talukdar S, et al. (2011) Brain PPAR-gamma promotes obesity and is required for the insulin-sensitizing effect of thiazolidinediones. Nat Med 17, 618-622