Dietary lipids do not contribute to the higher hepatic triglyceride levels of fructose-compared to glucose-fed mice

FASEB Journal

Volumn 28, Issue 5, 2014, Pages 1988-1997

  Nunes, Patricia M ^a,c   Wright, Alan J ^a   Veltien, Andor ^a   Van Asten, Jack J A ^a   Tack, Cees J ^a   Jones, John G ^b   Heerschap, Arend ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

De novo lipogenesis; In vivo hepatic lipid metabolism; Magnetic resonance spectroscopy

Indexed keywords

ADENOSINE TRIPHOSPHATE; FATTY ACID; FRUCTOSE; GLUCOSE; INSULIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ABDOMINAL FAT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CARBON NUCLEAR MAGNETIC RESONANCE; CLEARANCE; COMPARATIVE STUDY; CONTROLLED STUDY; FAT INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE INTAKE; GLUCOSE TOLERANCE; HOMEOSTASIS; INSULIN BLOOD LEVEL; INSULIN TOLERANCE TEST; LIPID ABSORPTION; LIPID LIVER LEVEL; MALE; METABOLIC FLUX ANALYSIS; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROMETER; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; WEIGHT GAIN;

DE NOVO LIPOGENESIS; IN VIVO HEPATIC LIPID METABOLISM; MAGNETIC RESONANCE SPECTROSCOPY;

ABSORPTION; ADENOSINE TRIPHOSPHATE; ADIPOSE TISSUE; ANIMALS; BLOOD GLUCOSE; DIET; DIETARY FATS; ENTEROCYTES; FRUCTOSE; GLUCOSE; LIPOGENESIS; LIVER; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MICE, INBRED C57BL; TRIGLYCERIDES;

EID: 84901049783     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-241208     Document Type: Article

References (37)

1. Bray, G. A. (2010) Fructose: pure, white, and deadly? Fructose, by any other name, is a health hazard. J. Diabetes Sci. Technol. 4, 1003-1007
2. Stanhope, K. L., Schwarz, J. M., Keim, N. L., Griffen, S. C., Bremer, A. A., Graham, J. L., Hatcher, B., Cox, C. L., Dyachenko, A., Zhang, W., McGahan, J. P., Seibert, A., Krauss, R. M., Chiu, S., Schaefer, E. J., Ai, M., Otokozawa, S., Nakajima, K., Nakano, T., Beysen, C., Hellerstein, M. K., Berglund, L., and Havel, P. J. (2009) Consuming fructose-sweetened, not glucosesweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J. Clin. Invest. 119, 1322-1334
3. Swarbrick, M. M., Stanhope, K. L., Elliott, S. S., Graham, J. L., Krauss, R. M., Christiansen, M. P., Griffen, S. C., Keim, N. L., and Havel, P. J. (2008) Consumption of fructose-sweetened beverages for 10 weeks increases postprandial triacylglycerol and apolipoprotein-B concentrations in overweight and obese women. Br. J. Nutr. 100, 947-952
4. Teff, K. L., Grudziak, J., Townsend, R. R., Dunn, T. N., Grant, R. W., Adams, S. H., Keim, N. L., Cummings, B. P., Stanhope, K. L., and Havel, P. J. (2009) 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. 94, 1562-1569
5. Ouyang, X., Cirillo, P., Sautin, Y., McCall, S., Bruchette, J. L., Diehl, A. M., Johnson, R. J., and Abdelmalek, M. F. (2008) Fructose consumption as a risk factor for non-alcoholic fatty liver disease. J. Hepatol. 48, 993-999
6. Assy, N., Nasser, G., Kamayse, I., Nseir, W., Beniashvili, Z., Djibre, A., and Grosovski, M. (2008) Soft drink consumption linked with fatty liver in the absence of traditional risk factors. Can. J. Gastroenterol. 22, 811-816
7. Abdelmalek, M. F., Suzuki, A., Guy, C., Unalp-Arida, A., Colvin, R., Johnson, R. J., and Diehl, A. M. (2010) Increased fructose consumption is associated with fibrosis severity in patients with nonalcoholic fatty liver disease. Hepatology 51, 1961-1971
8. Koo, H. Y., Wallig, M. A., Chung, B. H., Nara, T. Y., Cho, B. H., and Nakamura, M. T. (2008) Dietary fructose induces a wide range of genes with distinct shift in carbohydrate and lipid metabolism in fed and fasted rat liver. Biochim. Biophys. Acta 1782, 341-348
9. Vila, L., Roglans, N., Perna, V., Sanchez, R. M., Vazquez-Carrera, M., Alegret, M., and Laguna, J. C. (2011) Liver AMP/ATP ratio and fructokinase expression are related to gender differences in AMPK activity and glucose intolerance in rats ingesting liquid fructose. J. Nutr. Biochem. 22, 741-751
10. Le, K. A., Ith, M., Kreis, R., Faeh, D., Bortolotti, M., Tran, C., Boesch, C., and Tappy, L. (2009) Fructose overconsumption causes dyslipidemia and ectopic lipid deposition in healthy subjects with and without a family history of type 2 diabetes. Am. J. Clin. Nutr. 89, 1760-1765
11. Tappy, L., and Le, K. A. (2010) Metabolic effects of fructose and the worldwide increase in obesity. Physiol. Rev. 90, 23-46
12. Roglans, N., Vila, L., Farre, M., Alegret, M., Sanchez, R. M., Vazquez-Carrera, M., and Laguna, J. C. (2007) Impairment of hepatic Stat-3 activation and reduction of PPARalpha activity in fructose-fed rats. Hepatology 45, 778-788
13. Hellerstein, M. K., Schwarz, J. M., and Neese, R. A. (1996) Regulation of hepatic de novo lipogenesis in humans. Annu. Rev. Nutr. 16, 523-557
14. Haidari, M., Leung, N., Mahbub, F., Uffelman, K. D., Kohen-Avramoglu, R., Lewis, G. F., and Adeli, K. (2002) Fasting and postprandial overproduction of intestinally derived lipoproteins in an animal model of insulin resistance. Evidence that chronic fructose feeding in the hamster is accompanied by enhanced intestinal de novo lipogenesis and ApoB48-containing lipoprotein overproduction. J. Biol. Chem. 277, 31646-31655
15. Lewis, G. F., Uffelman, K., Naples, M., Szeto, L., Haidari, M., and Adeli, K. (2005) Intestinal lipoprotein overproduction, a newly recognized component of insulin resistance, is ameliorated by the insulin sensitizer rosiglitazone: studies in the fructose-fed Syrian golden hamster. Endocrinology 146, 247-255
16. Griffiths, J. R., Stevens, A. N., Gadian, D. G., Iles, R. A., and Porteous, R. (1980) Hepatic fructose metabolism studied by 31P nuclear magnetic resonance in the anaesthetized rat. Biochem. Soc. Trans. 8, 641
17. Abdelmalek, M. F., Lazo, M., Horska, A., Bonekamp, S., Lipkin, E. W., Balasubramanyam, A., Bantle, J. P., Johnson, R. J., Diehl, A. M., and Clark, J. M. (2012) Higher dietary fructose is associated with impaired hepatic adenosine triphosphate homeostasis in obese individuals with type 2 diabetes. Hepatology 56, 952-960
18. Nunes, P. M., van de Weijer, T., Veltien, A., Arnts, H., Hesselink, M. K. C., Glatz, J. F. C., Schrauwen, P., Tack, C. J., and Heerschap, A. (2012) Increased intramyocellular lipids but unaltered in vivo mitochondrial oxidative phosphorylation in skeletal muscle of adipose triglyceride lipase-deficient mice. Am. J. Physiol. Endocrinol. Metab. 303, E71-E81
19. Staewen, R. S., Johnson, A. J., Ross, B. D., Parrish, T., Merkle, H., and Garwood, M. (1990) 3-D FLASH imaging using a single surface coil and a new adiabatic pulse, BIR-4. Invest. Radiol. 25, 559-567
20. Vanhamme, L., van den, B. A., and Van, H. S. (1997) Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J. Magn. Reson. 129, 35-43
21. Naressi, A., Couturier, C., Devos, J. M., Janssen, M., Mangeat, C., de, B. R., and Graveron-Demilly, D. (2001) Java-based graphical user interface for the MRUI quantitation package. MAGMA 12, 141-152
22. Chemlik, M., Kukurova, I. J., Gruber, S., Krssak, M., Tkacov, M., Valkovic, L., Siegfried, T., and Wolfgang, B. (2012) T1 relaxation times of 31P metabolites in human liver at 7T. In Proc. Intl. Soc. Mag. Reson. Med. 20, 1704 (abstr.)
23. Moon, R. B., and Richards, J. H. (1973) Determination of intracellular pH by 31P magnetic resonance. J. Biol. Chem. 248, 7276-7278
24. Pfeuffer, J., Tkac, I., Choi, I. Y., Merkle, H., Ugurbil, K., Garwood, M., and Gruetter, R. (1999) Localized in vivo 1H NMR detection of neurotransmitter labeling in rat brain during infusion of [1-13C] D-glucose. Magn. Reson. Med. 41, 1077-1083
25. Jonkers, R. A. M., Geraedts, T. R., van Loon, L. J. C., Nicolay, K., and Prompers, J. J. (2012) Multitissue assessment of in vivo postprandial intracellular lipid partitioning in rats using localized 1H-[13C] magnetic resonance spectroscopy. Magn. Reson. Med. 68, 997-1006
26. Jonkers, R. A., van Loon, L. J., Nicolay, K., and Prompers, J. J. (2013) In vivo postprandial lipid partitioning in liver and skeletal muscle in prediabetic and diabetic rats. Diabetologia 56
27. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509
28. Delgado, T. C., Pinheiro, D., Caldeira, M., Castro, M. M., Geraldes, C. F., Lopez-Larrubia, P., Cerdan, S., and Jones, J. G. (2009) Sources of hepatic triglyceride accumulation during high-fat feeding in the healthy rat. NMR Biomed. 22, 310-317
29. Jones, J. G., Merritt, M., and Malloy, C. (2001) Quantifying tracer levels of (2)H(2)O enrichment from microliter amounts of plasma and urine by (2)H NMR. Magn. Reson. Med. 45, 156-158
30. Kasim-Karakas, S. E., Vriend, H., Almario, R., Chow, L.-C., and Goodman, M. N. (1996) Effects of dietary carbohydrates on glucose and lipid metabolism in golden Syrian hamsters. J. Lab. Clin. Med. 128, 208-213
31. Thorburn, A. W., Storlien, L. H., Jenkins, A. B., Khouri, S., and Kraegen, E. W. (1989) Fructose-induced in vivo insulin resistance and elevated plasma triglyceride levels in rats. Am. J. Clin. Nutr. 49, 1155-1163
32. Rizkalla, S., Luo, J., Guilhem, I., Boillot, J., Bruzzo, F., Chevalier, A., and Slama, G. (1992) Comparative effects of 6 week fructose, dextrose and starch feeding on fat-cell lipolysis in normal rats: effects of isoproterenol, theophylline and insulin. Mol. Cell. Biochem. 109, 127-132
33. Ngo Sock, E. T., Le, K. A., Ith, M., Kreis, R., Boesch, C., and Tappy, L. (2010) Effects of a short-term overfeeding with fructose or glucose in healthy young males. Br. J. Nutr. 103, 939-943
34. Elliott, S. S., Keim, N. L., Stern, J. S., Teff, K., and Havel, P. J. (2002) Fructose, weight gain, and the insulin resistance syndrome. Am. J. Clin. Nutr. 76, 911-922
35. Sevastianova, K., Hakkarainen, A., Kotronen, A., Corner, A., Arkkila, P., Arola, J., Westerbacka, J., Bergholm, R., Lundbom, J., Lundbom, N., and Yki-Jarvinen, H. (2010) Nonalcoholic fatty liver disease: detection of elevated nicotinamide adenine dinucleotide phosphate with in vivo 3.0-T 31P MR spectroscopy with proton decoupling. Radiology 256, 466-473
36. Taghibiglou, C., Rashid-Kolvear, F., Van Iderstine, S. C., Le-Tien, H., Fantus, I. G., Lewis, G. F., and Adeli, K. (2002) Hepatic very low density lipoprotein-ApoB overproduction is associated with attenuated hepatic insulin signaling and overexpression of protein-tyrosine phosphatase 1B in a fructose-fed hamster model of insulin resistance. J. Biol. Chem. 277, 793-803
37. Higuchi, K., Kitagawa, K., Kogishi, K., and Takeda, T. (1992) Developmental and age-related changes in apolipoprotein B mRNA editing in mice. J. Lipid Res. 33, 1753-1764