Pasture v. standard dairy cream in high-fat diet-fed mice: Improved metabolic outcomes and stronger intestinal barrier

British Journal of Nutrition

Volumn 112, Issue 4, 2014, Pages 520-535

  Benoit, Bérengère ^a,b   Plaisancié, Pascale ^b,c   Géloën, Alain ^b   Estienne, Monique ^b,c   Debard, Cyrille ^c   Meugnier, Emmanuelle ^c   Loizon, Emmanuelle ^c   Daira, Patricia ^b   Bodennec, Jacques ^a   Cousin, Olivier ^d   Vidal, Hubert ^c,e   Laugerette, Fabienne ^a   Michalski, Marie Caroline ^b,c,e  

^a UNIVERSITÉ LYON 1   (France)

^b Univ Lyon   (France)

^c CarMeN   (France)

^d Sodiaal Candia RandD   (France)

^e CENS   (France)

Author keywords

Dairy products; Fatty acid profiles; Gut barrier; HT29 MTX cells; Intestinal goblet cells; Lipid metabolism

Indexed keywords

LINOLENIC ACID; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TRIACYLGLYCEROL; UNCOUPLING PROTEIN 2; CARNITINE PALMITOYLTRANSFERASE I; CD36 ANTIGEN; CD68 ANTIGEN; DIACYLGLYCEROL ACYLTRANSFERASE 1; GLYCOPROTEIN P 15095; HORMONE SENSITIVE LIPASE; INTERLEUKIN 6; LINOLEIC ACID; LIPOPROTEIN LIPASE; MONOCYTE CHEMOTACTIC PROTEIN 1; MUCIN 2; TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL LIPASE; TUMOR NECROSIS FACTOR ALPHA;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; BODY WEIGHT; CELL POPULATION; COLON; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DAIRY PRODUCT; DUODENUM; FAT MASS; FOOD INTAKE; GENE; GENE EXPRESSION; GOBLET CELL; HUMAN; HUMAN CELL; INFLAMMATION; INTESTINE EPITHELIUM; INTESTINE FUNCTION; JEJUNUM; LIPID DIET; LIPID METABOLISM; LIVER; MALE; MOUSE; NONHUMAN; PANETH CELL; PASTURE DAIRY CREAM; PLASMA; PPARALPHA GENE; PROTEIN EXPRESSION; SMALL INTESTINE; STANDARD DAIRY CREAM; WEIGHT GAIN; WHITE ADIPOSE TISSUE; INTESTINAL BARRIER; METABOLISM;

ANIMALIA; MUS;

ADIPOSE TISSUE, WHITE; ANIMAL HUSBANDRY; ANIMALS; CATTLE; DAIRY PRODUCTS; DIET; DIET, HIGH-FAT; DIETARY FATS; FEMALE; FUNCTIONAL FOOD; HYPERTRIGLYCERIDEMIA; INTESTINAL MUCOSA; LIVER; MALE; MICE; MICE, INBRED C57BL; MILK; OBESITY; PANNICULITIS; PLANT COMPONENTS, AERIAL; POACEAE; RANDOM ALLOCATION;

EID: 84905593030     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114514001172     Document Type: Article

References (78)

1. Siri-Tarino PW, Sun Q, Hu FB, et al. (2010) Saturated fatty acids and risk of coronary heart disease: Modulation by replacement nutrients. Curr Atheroscler Rep 12, 384-390.
2. van Dijk SJ, Feskens EJ, Bos MB, et al. (2009) A saturated fatty acid-rich diet induces an obesity-linked proinflammatory gene expression profile in adipose tissue of subjects at risk of metabolic syndrome. Am J Clin Nutr 90, 1656-1664.
3. Lichtenstein AH, Appel LJ, Brands M, et al. (2006) Diet and lifestyle recommendations revision 2006: A scientific statement from the American Heart Association Nutrition Committee. Circulation 114, 82-96.
4. British Nutrition Foundation (2004). Nutrient Requirements and Recommendations. London: British Nutrition Foundation.
5. Australian National Health and Medical Research Council (2003) Food for Health: Dietary Guidelines for Australians: A Guide to Healthy Eating. Canberra, ACT: Department of Health and Ageing, Australian Government.
6. Jensen RG, Ferris AM & Lammi-Keefe CJ (1991) The composition of milk fat. J Dairy Sci 74, 3228-3243.
7. Rouillé B & Montourcy M (2010) Influence of French dairy feeding systems on cow milk fatty acid composition. Grassl Sci Eur 15, 619-621.
8. Chen SC, Lin YH, Huang HP, et al. (2012) Effect of conjugated linoleic acid supplementation on weight loss and body fat composition in a Chinese population. Nutrition 28, 559-565.
9. Whigham LD, Watras AC & Schoeller DA (2007) Efficacy of conjugated linoleic acid for reducing fat mass: A metaanalysis in humans. Am J Clin Nutr 85, 1203-1211.
10. Baranowski M, Enns J, Blewett H, et al. (2012) Dietary flaxseed oil reduces adipocyte size, adipose monocyte chemoattractant protein-1 levels and T-cell infiltration in obese, insulin-resistant rats. Cytokine 59, 382-391.
11. Norris LE, Collene AL, Asp ML, et al. (2009) Comparison of dietary conjugated linoleic acid with safflower oil on body composition in obese postmenopausal women with type 2 diabetes mellitus. Am J Clin Nutr 90, 468-476.
12. de Luis DA, de la Fuente B, Izaola O, et al. (2011) Double blind randomized clinical trial controlled by placebo with an alpha linoleic acid and prebiotic enriched cookie on risk cardiovascular factor in obese patients. Nutr Hosp 26, 827-833.
13. Roy A, Chardigny JM, Bauchart D, et al. (2007) Butters rich either in trans-10-C18:1 or in trans-11-C18:1 plus cis-9, trans-11 CLA differentially affect plasma lipids and aortic fatty streak in experimental atherosclerosis in rabbits. Animal 1, 467-476.
14. Valeille K, Ferezou J, Parquet M, et al. (2006) The natural concentration of the conjugated linoleic acid, cis-9, trans-11, in milk fat has antiatherogenic effects in hyperlipidemic hamsters. J Nutr 136, 1305-1310.
15. Seidel C, Deufel T & Jahreis G (2005) Effects of fat-modified dairy products on blood lipids in humans in comparison with other fats. Ann Nutr Metab 49, 42-48.
16. Malpuech-Brugere C, Mouriot J, Boue-Vaysse C, et al. (2010) Differential impact of milk fatty acid profiles on cardiovascular risk biomarkers in healthy men and women. Eur J Clin Nutr 64, 752-759.
17. Wellen KE & Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115, 1111-1119.
18. Laugerette F, Furet JP, Debard C, et al. (2012) Oil composition of high-fat diet affects metabolic inflammation differently in connection with endotoxin receptors in mice. Am J Physiol Endocrinol Metab 302, E374-E386.
19. Nguyen P, Leray V, Diez M, et al. (2008) Liver lipid metabolism. J Anim Physiol Anim Nutr (Berl) 92, 272-283.
20. Pyper SR, Viswakarma N, Yu S, et al. (2010) PPARa: Energy combustion, hypolipidemia, inflammation and cancer. Nucl Recept Signal 8, e002.
21. de Wit NJ, Bosch-Vermeulen H, de Groot PJ, et al. (2008) The role of the small intestine in the development of dietary fat-induced obesity and insulin resistance in C57BL/6J mice. BMC Med Genomics 1, 14.
22. Kondo H, Minegishi Y, Komine Y, et al. (2006) Differential regulation of intestinal lipid metabolism-related genes in obesity-resistant A/J vs obesity-prone C57BL/6J mice. Am J Physiol Endocrinol Metab 291, E1092-E1099.
23. Ley RE, Backhed F, Turnbaugh P, et al. (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102, 11070-11075.
24. Turnbaugh PJ & Gordon JI (2009) The core gut microbiome, energy balance and obesity. J Physiol 587, 4153-4158.
25. Petit V, Arnould L, Martin P, et al. (2007) Chronic high-fat diet affects intestinal fat absorption and postprandial triglyceride levels in the mouse. J Lipid Res 48, 278-287.
26. Cani PD, Bibiloni R, Knauf C, et al. (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57, 1470-1481.
27. Allen A, Hutton DA & Pearson JP (1998) The MUC2 gene product: A human intestinal mucin. Int J Biochem Cell Biol 30, 797-801.
28. Dekker J, Rossen JW, Buller HA, et al. (2002) The MUC family: An obituary. Trends Biochem Sci 27, 126-131.
29. Bevins CL & Salzman NH (2011) Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 9, 356-368.
30. Ouellette AJ (2011) Paneth cell a-defensins in enteric innate immunity. Cell Mol Life Sci 68, 2215-2229.
31. Park PW & Goins RE (1994) In situ preparation of fatty acid methyl esters for analysis of fatty acid composition in foods. J Food Sci 59, 1262-1266.
32. Benoit B, Fauquant C, Daira P, et al. (2010) Phospholipid species and minor sterols in French human milks. Food Chem 120, 684-691.
33. 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.
34. Bartlett GR (1959) Phosphorus assay in column chromatography. J Biol Chem 234, 466-468.
35. Buccoliero R, Bodennec J, Van Echten-Deckert G, et al. (2004) Phospholipid synthesis is decreased in neuronal tissue in a mouse model of Sandhoff disease. J Neurochem 90, 80-88.
36. Lefils J, Geloen A, Vidal H, et al. (2010) Dietary DHA: Time course of tissue uptake and effects on cytokine secretion in mice. Br J Nutr 104, 1304-1312.
37. Estienne M, Claustre J, Clain-Gardechaux G, et al. (2010) Maternal deprivation alters epithelial secretory cell lineages in rat duodenum: Role of CRF-related peptides. Gut 59, 744-751.
38. Cani PD, Amar J, Iglesias MA, et al. (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761-1772.
39. Abumrad NA & Davidson NO (2012) Role of the gut in lipid homeostasis. Physiol Rev 92, 1061-1085.
40. Lee B, Fast AM, Zhu J, et al. (2010) Intestine-specific expression of acyl CoA:diacylglycerol acyltransferase 1 reverses resistance to diet-induced hepatic steatosis and obesity in Dgat12/2 mice. J Lipid Res 51, 1770-1780.
41. Lefebvre P, Chinetti G, Fruchart JC, et al. (2006) Sorting out the roles of PPARa in energy metabolism and vascular homeostasis. J Clin Invest 116, 571-580.
42. Sampath H & Ntambi JM (2004) Polyunsaturated fatty acid regulation of gene expression. Nutr Rev 62, 333-339.
43. Gonzalez-Manan D, Tapia G, Gormaz JG, et al. (2012) Bioconversion of a-linolenic acid to n-3 LCPUFA and expression of PPAR-a, acyl coenzyme A oxidase 1 and carnitine acyl transferase I are incremented after feeding rats with a-linolenic acid-rich oils. Food Funct 3, 765-772.
44. Moya-Camarena SY, Vanden Heuvel JP, Blanchard SG, et al. (1999) Conjugated linoleic acid is a potent naturally occurring ligand and activator of PPARa. J Lipid Res 40, 1426-1433.
45. Konig B, Spielmann J, Haase K, et al. (2008) Effects of fish oil and conjugated linoleic acids on expression of target genes of PPARa and sterol regulatory element-binding proteins in the liver of laying hens. Br J Nutr 100, 355-363.
46. House RL, Cassady JP, Eisen EJ, et al. (2005) Functional genomic characterization of delipidation elicited by trans-10, cis-12-conjugated linoleic acid (t10c12-CLA) in a polygenic obese line of mice. Physiol Genomics 21, 351-361.
47. Hur SJ, Kim DH, Chun SC, et al. (2013) Effects of dietary conjugated linoleic acid and biopolymer encapsulation on lipid metabolism in mice. Int J Mol Sci 14, 6848-6862.
48. Choi JS, Koh IU, Jung MH, et al. (2007) Effects of three different conjugated linoleic acid preparations on insulin signalling, fat oxidation and mitochondrial function in rats fed a high-fat diet. Br J Nutr 98, 264-275.
49. Jump DB, Clarke SD, Thelen A, et al. (1994) Coordinate regulation of glycolytic and lipogenic gene expression by polyunsaturated fatty acids. J Lipid Res 35, 1076-1084.
50. Fleury C, Neverova M, Collins S, et al. (1997) Uncoupling protein-2: A novel gene linked to obesity and hyperinsulinemia. Nat Genet 15, 269-272.
51. House RL, Cassady JP, Eisen EJ, et al. (2005) Conjugated linoleic acid evokes delipidation through the regulation of genes controlling lipid metabolism in adipose and liver tissue. Obes Rev 6, 247-258.
52. Libby P (2002) Inflammation in atherosclerosis. Nature 420, 868-874.
53. Weisberg SP, McCann D, Desai M, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112, 1796-1808.
54. McClelland S, Cox C, O'Connor R, et al. (2010) Conjugated linoleic acid suppresses the migratory and inflammatory phenotype of the monocyte/macrophage cell. Atherosclerosis 211, 96-102.
55. Orgaard A & Jensen L (2008) The effects of soy isoflavones on obesity. Exp Biol Med (Maywood) 233, 1066-1080.
56. Chen SW, Zhang LS, Zhang HM, et al. (2006) Effects of soy isoflavone on levels of low-grade inflammatory peptides in rats with insulin resistance. Nan Fang Yi Ke Da Xue Xue Bao 26, 1484-1486.
57. Yanagisawa M, Sugiya M, Iijima H, et al. (2012) Genistein and daidzein, typical soy isoflavones, inhibit TNF-amediated downregulation of adiponectin expression via different mechanisms in 3T3-L1 adipocytes. Mol Nutr Food Res 56, 1783-1793.
58. Clevers HC & Bevins CL (2013) Paneth cells: Maestros of the small intestinal crypts. Annu Rev Physiol 75, 289-311.
59. McGuckin MA, Linden SK, Sutton P, et al. (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9, 265-278.
60. Deplancke B & Gaskins HR (2001) Microbial modulation of innate defense: Goblet cells and the intestinal mucus layer. Am J Clin Nutr 73, 1131S-1141S.
61. Desai MA, Mutlu M & Vadgama P (1992) A study of macromolecular diffusion through native porcine mucus. Experientia 48, 22-26.
62. Hodin CM, Verdam FJ, Grootjans J, et al. (2011) Reduced Paneth cell antimicrobial protein levels correlate with activation of the unfolded protein response in the gut of obese individuals. J Pathol 225, 276-284.
63. Barcelo A, Claustre J, Toumi F, et al. (2001) Effect of bile salts on colonic mucus secretion in isolated vascularly perfused rat colon. Dig Dis Sci 46, 1223-1231.
64. Claustre J,Toumi F, Trompette A, et al. (2002) Effects of peptides derived from dietary proteins on mucus secretion in rat jejunum. Am J Physiol Gastrointest Liver Physiol 283, G521-G528.
65. Trompette A, Claustre J, Caillon F, et al. (2003) Milk bioactive peptides and b-casomorphins induce mucus release in rat jejunum. J Nutr 133, 3499-3503.
66. Plaisancie P, Claustre J, Estienne M, et al. (2013) A novel bioactive peptide from yoghurts modulates expression of the gel-forming MUC2 mucin as well as population of goblet cells and Paneth cells along the small intestine. J Nutr Biochem 24, 213-221.
67. Nicholson JK, Holmes E, Kinross J, et al. (2012) Host-gut microbiota metabolic interactions. Science 336, 1262-1267.
68. Chang M, Alsaigh T, Kistler EB, et al. (2012) Breakdown of mucin as barrier to digestive enzymes in the ischemic rat small intestine. PLOS ONE 7, e40087.
69. Iiboshi Y, Nezu R, Kennedy M, et al. (1994) Total parenteral nutrition decreases luminal mucous gel and increases permeability of small intestine. J Parenter Enteral Nutr 18, 346-350.
70. Fuse K, Bamba T & Hosoda S (1989) Effects of pectin on fatty acid and glucose absorption and on thickness of unstirred water layer in rat and human intestine. Dig Dis Sci 34, 1109-1116.
71. Mayer RM, Treadwell CR, Gallo LL, et al. (1985) Intestinal mucins and cholesterol uptake in vitro. Biochim Biophys Acta 833, 34-43.
72. Choi JS, Kim H, Jung MH, et al. (2010) Consumption of barley b-glucan ameliorates fatty liver and insulin resistance in mice fed a high-fat diet. Mol Nutr Food Res 54, 1004-1013.
73. Brockman DA, Chen X & Gallaher DD (2013) Consumption of a high b-glucan barley flour improves glucose control and fatty liver and increases muscle acylcarnitines in the Zucker diabetic fatty rat. Eur J Nutr 52, 1743-1753.
74. Poulet JL, Fraisse D, Viala D, et al. (2002) Flavonoids in forages: Composition and possible effects on milk quality. Proceedings of the 19th General Meeting of the European Grassland Federation. Grassl Sci Eur 7, 590-591.
75. Misawa E, Tanaka M, Nomaguchi K, et al. (2008) Administration of phytosterols isolated from Aloe vera gel reduce visceral fat mass and improve hyperglycemia in Zucker diabetic fatty (ZDF) rats. Obes Res Clin Pract 2, I-II.
76. Micallef MA & Garg ML (2008) The lipid-lowering effects of phytosterols and (n-3) polyunsaturated fatty acids are synergistic and complementary in hyperlipidemic men and women. J Nutr 138, 1086-1090.
77. Nakagawa K, Kishida H, Arai N, et al. (2004) Licorice flavonoids suppress abdominal fat accumulation and increase in blood glucose level in obese diabetic KK-A(y) mice. Biol Pharm Bull 27, 1775-1778.
78. Kamisoyama H,Honda K, Tominaga Y, et al. (2008) Investigation of the anti-obesity action of licorice flavonoid oil in diet-induced obese rats. Biosci Biotechnol Biochem 72, 3225-3231.