Acute dietary fat intake initiates alterations in energy metabolism and insulin resistance

Journal of Clinical Investigation

Volumn 127, Issue 2, 2017, Pages 695-708

  Hernández, Elisa Alvarez ^a,b   Kahl, Sabine ^a,b   Seelig, Anett ^c   Begovatz, Paul ^a,b   Irmler, Martin ^c   Kupriyanova, Yuliya ^a,b   Nowotny, Bettina ^a,b,g   Nowotny, Peter ^a,b   Herder, Christian ^a,b   Barosa, Cristina ^d   Carvalho, Filipa ^d   Rozman, Jan ^c   Neschen, Susanne ^b,c,h   Jones, John G ^d,e   Beckers, Johannes ^b,c,f   De Angelis, Martin Hrabě ^b,c,f   Roden, Michael ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e APDP Portuguese Diabetes Association   (Portugal)

^f TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^g CRS Clinical Research Services GmbH   (Germany)

^h SANOFI AVENTIS DEUTSCHLAND GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; LIPOPOLYSACCHARIDE; PALM OIL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; SATURATED FATTY ACID; TOLL LIKE RECEPTOR; TRANSCRIPTOME; TRIACYLGLYCEROL; FAT INTAKE; TNFSF12 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR; VEGETABLE OIL;

ADIPOSE TISSUE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; ENERGY METABOLISM; EX VIVO STUDY; FAT INTAKE; GLUCONEOGENESIS; GLUCOSE METABOLISM; GLYCOGENOLYSIS; HUMAN; HUMAN EXPERIMENT; HYPERINSULINEMIC-EUGLYCEMIC CLAMP TECHNIQUE; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; ISOTOPE DILUTION ASSAY; LEAN BODY WEIGHT; LIPID METABOLISM; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RANDOMIZED CONTROLLED TRIAL; ADMINISTRATION AND DOSAGE; ADVERSE EFFECTS; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; LIVER; METABOLISM; PATHOLOGY;

ADIPOSE TISSUE; ADULT; ANIMALS; DIETARY FATS; ENERGY METABOLISM; HUMANS; INSULIN RESISTANCE; LIVER; MALE; MICE; NF-KAPPA B; NON-ALCOHOLIC FATTY LIVER DISEASE; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; PLANT OILS; TUMOR NECROSIS FACTORS;

EID: 85014086154     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI89444     Document Type: Article

References (72)

1. van Dam RM, Willett WC, Rimm EB, Stampfer MJ, Hu FB. Dietary fat and meat intake in relation to risk of type 2 diabetes in men. Diabetes Care. 2002;25(3):417-424.
2. Mancini A, et al. Biological and Nutritional Properties of Palm Oil and Palmitic Acid: Effects on Health. Molecules. 2015;20(9):17339-17361.
3. Szendroedi J, et al. Abnormal hepatic energy homeostasis in type 2 diabetes. Hepatology. 2009;50(4):1079-1086.
4. Koliaki C, Roden M. Hepatic energy metabolism in human diabetes mellitus, obesity and nonalcoholic fatty liver disease. Mol Cell Endocrinol. 2013;379(1-2):35-42.
5. Erion DM, Shulman GI. Diacylglycerol-mediated insulin resistance. Nat Med. 2010;16(4):400-402.
6. Magkos F, et al. Effects of Moderate and Subsequent Progressive Weight Loss on Metabolic Function and Adipose Tissue Biology in Humans with Obesity. Cell Metab. 2016;23(4):591-601.
7. Winzell MS, Ahrén B. The high-fat diet-fed mouse: A model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes. 2004;53 Suppl 3:S215-S219.
8. Gastaldelli A, et al. Influence of obesity and type 2 diabetes on gluconeogenesis and glucose output in humans: A quantitative study. Diabetes. 2000;49(8):1367-1373.
9. Groop LC, et al. Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus. Evidence for multiple sites of insulin resistance. J Clin Invest. 1989;84(1):205-213.
10. Lewis GF, Carpentier A, Vranic M, Giacca A. Resistance to insulin's acute direct hepatic effect in suppressing steady-state glucose production in individuals with type 2 diabetes. Diabetes. 1999;48(3):570-576.
11. Bachmann OP, et al. Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes. 2001;50(11):2579-2584.
12. Roden M, et al. Mechanism of free fatty acidinduced insulin resistance in humans. J Clin Invest. 1996;97(12):2859-2865.
13. Szendroedi J, et al. Lipid-induced insulin resistance is not mediated by impaired transcapillary transport of insulin and glucose in humans. Diabetes. 2012;61(12):3176-3180.
14. Itani SI, Ruderman NB, Schmieder F, Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes. 2002;51(7):2005-2011.
15. Kashyap SR, et al. Discordant effects of a chronic physiological increase in plasma FFA on insulin signaling in healthy subjects with or without a family history of type 2 diabetes. Am J Physiol Endocrinol Metab. 2004;287(3):E537-E546.
16. Boden G, et al. Effects of fat on insulinstimulated carbohydrate metabolism in normal men. J Clin Invest. 1991;88(3):960-966.
17. Shah P, et al. Effects of free fatty acids and glycerol on splanchnic glucose metabolism and insulin extraction in nondiabetic humans. Diabetes. 2002;51(2):301-310.
18. Clore JN, Stillman JS, Li J, O'Keefe SJ, Levy JR. Differential effect of saturated and polyunsaturated fatty acids on hepatic glucose metabolism in humans. Am J Physiol Endocrinol Metab. 2004;287(2):E358-E365.
19. Nowotny B, et al. Mechanisms underlying the onset of oral lipid-induced skeletal muscle insulin resistance in humans. Diabetes. 2013;62(7):2240-2248.
20. Xiao C, Giacca A, Carpentier A, Lewis GF. Differential effects of monounsaturated, polyunsaturated and saturated fat ingestion on glucose-stimulated insulin secretion, sensitivity and clearance in overweight and obese, non-diabetic humans. Diabetologia. 2006;49(6):1371-1379.
21. Lee CG, Demarquoy J, Jackson MJ, O'Brien WE. Molecular cloning and characterization of a murine LPS-inducible cDNA. J Immunol. 1994;152(12):5758-5767.
22. Ban JY, Kim BS, Kim SC, Kim DH, Chung JH. Microarray Analysis of Gene Expression Profiles in Response to Treatment with Melatonin in Lipopolysaccharide Activated RAW 264.7 Cells. Korean J Physiol Pharmacol. 2011;15(1):23-29.
23. Li L, et al. A solute carrier family 22 member 3 variant rs3088442 G→A associated with coronary heart disease inhibits lipopolysaccharide-induced inflammatory response. J Biol Chem. 2015;290(9):5328-5340.
24. Sivapalaratnam S, et al. Identification of candidate genes linking systemic inflammation to atherosclerosis; results of a human in vivo LPS infusion study. BMC Med Genomics. 2011;4:64.
25. Masaki M, Ikeda A, Shiraki E, Oka S, Kawasaki T. Mixed lineage kinase LZK and antioxidant protein-1 activate NF-kappaB synergistically. Eur J Biochem. 2003;270(1):76-83.
26. Noh H, Paik HY, Kim J, Chung J. The alteration of zinc transporter gene expression is associated with inflammatory markers in obese women. Biol Trace Elem Res. 2014;158(1):1-8.
27. Westerbacka J, et al. Genes involved in fatty acid partitioning and binding, lipolysis, monocyte/macrophage recruitment, and inflammation are overexpressed in the human fatty liver of insulinresistant subjects. Diabetes. 2007;56(11):2759-2765.
28. Deopurkar R, et al. Differential effects of cream, glucose, and orange juice on inflammation, endotoxin, and the expression of Toll-like receptor-4 and suppressor of cytokine signaling-3. Diabetes Care. 2010;33(5):991-997.
29. Roden M, et al. Effects of free fatty acid elevation on postabsorptive endogenous glucose production and gluconeogenesis in humans. Diabetes. 2000;49(5):701-707.
30. Kacerovsky M, et al. Postprandial and fasting hepatic glucose fluxes in long-standing type 1 diabetes. Diabetes. 2011;60(6):1752-1758.
31. Hundal RS, et al. Mechanism by which metformin reduces glucose production in type 2 diabetes. Diabetes. 2000;49(12):2063-2069.
32. Wang L, et al. Acute stimulation of glucagon secretion by linoleic acid results from GPR40 activation and [Ca2+]i increase in pancreatic islet {alpha}-cells. J Endocrinol. 2011;210(2):173-179.
33. Roden M, et al. The roles of insulin and glucagon in the regulation of hepatic glycogen synthesis and turnover in humans. J Clin Invest. 1996;97(3):642-648.
34. Fritsch M, et al. Time course of postprandial hepatic phosphorus metabolites in lean, obese, and type 2 diabetes patients. Am J Clin Nutr. 2015;102(5):1051-1058.
35. Koliaki C, et al. Adaptation of hepatic mitochondrial function in humans with non-alcoholic fatty liver is lost in steatohepatitis. Cell Metab. 2015;21(5):739-746.
36. Schmid AI, Szendroedi J, Chmelik M, Krssák M, Moser E, Roden M. Liver ATP synthesis is lower and relates to insulin sensitivity in patients with type 2 diabetes. Diabetes Care. 2011;34(2):448-453.
37. Frayn KN. Adipose tissue as a buffer for daily lipid flux. Diabetologia. 2002;45(9):1201-1210.
38. Søndergaard E, Sørensen LP, Rahbek I, Gormsen LC, Christiansen JS, Nielsen S. Postprandial VLDL-triacylglycerol secretion is not suppressed in obese type 2 diabetic men. Diabetologia. 2012;55(10):2733-2740.
39. Perry RJ, Samuel VT, Petersen KF, Shulman GI. The role of hepatic lipids in hepatic insulin resistance and type 2 diabetes. Nature. 2014;510(7503):84-91.
40. Hennes MM, Shrago E, Kissebah AH. Receptor and postreceptor effects of free fatty acids (FFA) on hepatocyte insulin dynamics. Int J Obes. 1990;14(10):831-841.
41. Wiesenthal SR, et al. Free fatty acids impair hepatic insulin extraction in vivo. Diabetes. 1999;48(4):766-774.
42. Vallim T, Salter AM. Regulation of hepatic gene expression by saturated fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2010;82(4-6):211-218.
43. Maecker H, et al. TWEAK attenuates the transition from innate to adaptive immunity. Cell. 2005;123(5):931-944.
44. Burkly LC. TWEAK/Fn14 axis: The current paradigm of tissue injury-inducible function in the midst of complexities. Semin Immunol. 2014;26(3):229-236.
45. Lozano-Bartolomé J, et al. Reduced circulating levels of sTWEAK are associated with NAFLD and may affect hepatocyte triglyceride accumulation. Int J Obes (Lond). 2016;40(9):1337-1345.
46. Cani PD, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56(7):1761-1772.
47. Chicheportiche Y, Fossati-Jimack L, Moll S, Ibnou-Zekri N, Izui S. Down-regulated expression of TWEAK mRNA in acute and chronic inflammatory pathologies. Biochem Biophys Res Commun. 2000;279(1):162-165.
48. Wullaert A, van Loo G, Heyninck K, Beyaert R. Hepatic tumor necrosis factor signaling and nuclear factor-kappaB: effects on liver homeostasis and beyond. Endocr Rev. 2007;28(4):365-386.
49. Chang G, et al. Hepatic TLR4 signaling is activated by LPS from digestive tract during SARA, and epigenetic mechanisms contribute to enforced TLR4 expression. Oncotarget. 2015;6(36):38578-38590.
50. Tang F, Tang G, Xiang J, Dai Q, Rosner MR, Lin A. The absence of NF-kappaB-mediated inhibition of c-Jun N-terminal kinase activation contributes to tumor necrosis factor alpha-induced apoptosis. Mol Cell Biol. 2002;22(24):8571-8579.
51. Cai D, et al. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat Med. 2005;11(2):183-190.
52. Jelenik T, et al. Tissue-specific differences in the development of insulin resistance in a mouse model for type 1 diabetes. Diabetes. 2014;63(11):3856-3867.
53. Santos SH, et al. Oral Angiotensin-(1-7) prevented obesity and hepatic inflammation by inhibition of resistin/TLR4/MAPK/NF-κB in rats fed with high-fat diet. Peptides. 2013;46:47-52.
54. Marion V, et al. BBS-induced ciliary defect enhances adipogenesis, causing paradoxical higher-insulin sensitivity, glucose usage, and decreased inflammatory response. Cell Metab. 2012;16(3):363-377.
55. Zhang X, Xie X, Heckmann BL, Saarinen AM, Czyzyk TA, Liu J. Targeted disruption of G0/G1 switch gene 2 enhances adipose lipolysis, alters hepatic energy balance, and alleviates high-fat diet-induced liver steatosis. Diabetes. 2014;63(3):934-946.
56. Fan Y, et al. Mutations in a member of the Ras superfamily of small GTP-binding proteins causes Bardet-Biedl syndrome. Nat Genet. 2004;36(9):989-993.
57. Haytowitz DB, Pehrsson PR, Holden JM. The National Food and Nutrient Analysis Program: A decade of progress. J Food Compost Anal. 2008;21(S1):S94-S102.
58. Urban LE, Roberts SB, Fierstein JL, Gary CE, Lichtenstein AH. Sodium, saturated fat, and trans fat content per 1,000 kilocalories: temporal trends in fast-food restaurants, United States, 2000-2013. Prev Chronic Dis. 2014;11:E228.
59. Teff KL, et al. Endocrine and metabolic effects of consuming fructose-and glucose-sweetened beverages with meals in obese men and women: influence of insulin resistance on plasma triglyceride responses. J Clin Endocrinol Metab. 2009;94(5):1562-1569.
60. American Diabetes Association. 3. Foundations of Care and Comprehensive Medical Evaluation. Diabetes Care. 2016;39 Suppl 1:S23-S35.
61. Krssak M, et al. Alterations in postprandial hepatic glycogen metabolism in type 2 diabetes. Diabetes. 2004;53(12):3048-3056.
62. Beaudoin MS, Robinson LE, Graham TE. An oral lipid challenge and acute intake of caffeinated coffee additively decrease glucose tolerance in healthy men. J Nutr. 2011;141(4):574-581.
63. Gancheva S, et al. Variants in Genes Controlling Oxidative Metabolism Contribute to Lower Hepatic ATP Independent of Liver Fat Content in Type 1 Diabetes. Diabetes. 2016;65(7):1849-1857.
64. Jones JG, et al. NMR derivatives for quantification of 2H and 13C-enrichment of human glucuronide from metabolic tracers. J Carbohydr Chem. 2006;25(2-3):203-217.
65. Nowotny B, Nowotny PJ, Strassburger K, Roden M. Precision and accuracy of blood glucose measurements using three different instruments. Diabet Med. 2012;29(2):260-265.
66. Herder C, et al. Adiponectin may mediate the association between omentin, circulating lipids and insulin sensitivity: results from the KORA F4 study. Eur J Endocrinol. 2015;172(4):423-432.
67. Brehm A, Krssak M, Schmid AI, Nowotny P, Waldhäusl W, Roden M. Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes. 2006;55(1):136-140.
68. Jones J, Kahl S, Carvalho F, Barosa C, Roden M. Simplified analysis of acetaminophen glucuronide for quantifying gluconeogenesis and glycogenolysis using deuterated water. Anal Biochem. 2015;479:37-39.
69. Barosa C, Jones JG, Rizza R, Basu A, Basu R. Acetaminophen glucuronide and plasma glucose report identical estimates of gluconeogenesis and glycogenolysis for healthy and prediabetic subjects using the deuterated water method. Magn Reson Med. 2013;70(2):315-319.
70. Bischof MG, et al. Hepatic glycogen metabolism in type 1 diabetes after long-term near normoglycemia. Diabetes. 2002;51(1):49-54.
71. Kraegen EW, James DE, Jenkins AB, Chisholm DJ. Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am J Physiol. 1985;248(3 Pt 1):E353-E362.
72. Neschen S, et al. Prevention of hepatic steatosis and hepatic insulin resistance in mitochondrial acyl-CoA:glycerol-sn-3-phosphate acyltransferase 1 knockout mice. Cell Metab. 2005;2(1):55-65.