Higher dietary fructose is associated with impaired hepatic adenosine triphosphate homeostasis in obese individuals with type 2 diabetes

Hepatology

Volumn 56, Issue 3, 2012, Pages 952-960

  Abdelmalek, Manal F ^a   Lazo, Mariana ^b   Horska, Alena ^b   Bonekamp, Susanne ^b   Lipkin, Edward W ^d   Balasubramanyam, Ashok ^e   Bantle, John P ^f   Johnson, Richard J ^g   Diehl, Anna Mae ^a   Clark, Jeanne M ^b,c  

^a DUKE UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

^g UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ADENOSINE TRIPHOSPHATE; ASPARTATE AMINOTRANSFERASE; CREATININE; FRUCTOSE; HEMOGLOBIN A1C; INSULIN; METFORMIN; PHOSPHATE; URIC ACID;

ADULT; AGED; ALCOHOL CONSUMPTION; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BLOOD SAMPLING; CONTROLLED STUDY; DIABETIC PATIENT; DISEASE ASSOCIATION; DISEASE COURSE; FOOD FREQUENCY QUESTIONNAIRE; FOOD INTAKE; HUMAN; HYPERURICEMIA; INSULIN TREATMENT; MAJOR CLINICAL STUDY; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OBESITY; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN HOMEOSTASIS; RISK FACTOR; URIC ACID BLOOD LEVEL; WAIST CIRCUMFERENCE;

ADENOSINE TRIPHOSPHATE; DIABETES MELLITUS, TYPE 2; DIETARY CARBOHYDRATES; FEMALE; FRUCTOSE; HOMEOSTASIS; HUMANS; MALE; MIDDLE AGED; OBESITY; SWEETENING AGENTS;

EID: 84865552258     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.25741     Document Type: Article

References (43)

1. Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. HEPATOLOGY 2006; 43: S99-S112.
2. Bray GA, Nielsen SJ, Popkin BM. Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity. Am J Clin Nutr 2004; 79: 537-543.
3. Vos MB Kimmons JE, Gillespie C, Welsh J, Blanck HM. Dietary fructose consumption among US children and adults: the Third National Health and Nutrition Examination Survey. Medscape J Med 2008; 10: 160.
4. Putnam J, Allshouse JE. Food Consumption, Prices and Expenditures, 1970-1997. USDA Statistical Bulletin 965. Washington, DC: Food and Rural Economics Division, Economics Research Service, US Department of Agriculture; 1999.
5. French SA, Lin BH, Guthrie JF. National trends in soft drink consumption among children and adolescents age 6 to 17 years: prevalence, amounts, and sources, 1977/1978 to 1994/1998. J Am Diet Assoc 2003; 103: 1326-1331.
6. Ouyang X, Cirillo P, Sautin Y, McCall S, Bruchette JL, Diehl AM, et al. Fructose consumption as a risk factor for non-alcoholic fatty liver disease. J Hepatol 2008; 48: 993-999.
7. Nakagawa T, Hu H, Zharikov S, Tuttle KR, Short RA, Glushakova O, et al. A causal role for uric acid in fructose-induced metabolic syndrome. Am J Physiol Renal Physiol 2006; 290: F625-F631.
8. Perez-Pozo SE, Schold J, Nakagawa T, Sanchez-Lozada LG, Johnson RJ, Lillo JL. Excessive fructose intake induces the features of metabolic syndrome in healthy adult men: role of uric acid in the hypertensive response. Int J Obes (Lond) 2010; 34: 454-461.
9. Sanchez-Lozada LG, Mu W, Roncal C, Sautin YY, Abdelmalek M, Reungjui S, et al. Comparison of free fructose and glucose to sucrose in the ability to cause fatty liver. Eur J Nutr 2010; 49: 1-9.
10. Ackerman Z, Oron-Herman M, Grozovski M, Rosenthal T, Pappo O, Link G, Sela BA. Fructose-induced fatty liver disease: hepatic effects of blood pressure and plasma triglyceride reduction. Hypertension 2005; 45: 1012-1018.
11. Stanhope KL, Schwarz JM, Keim NL, Griffen SC, Bremer AA, Graham JL, et al. Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J Clin Invest 2009; 119: 1322-1334.
12. Schulze MB, Manson JE, Ludwig DS, Colditz GA, Stampfer MJ, Willett WC, Hu FB. Sugar-sweetened beverages, weight gain, and incidence of type 2 diabetes in young and middle-aged women. JAMA 2004; 292: 927-934.
13. Cave M, Deaciuc I, Mendez C, Song Z, Joshi-Barve S, Barve S, McClain C. Nonalcoholic fatty liver disease: predisposing factors and the role of nutrition. J Nutr Biochem 2007; 18: 184-195.
14. Abdelmalek MF, Suzuki A, Guy C, Unalp-Arida A, Colvin R, Johnson RJ, Diehl AM. Increased fructose consumption is associated with fibrosis severity in patients with nonalcoholic fatty liver disease. HEPATOLOGY 2010; 51: 1961-1971.
15. van den Berghe G, Bronfman M, Vanneste R, Hers HG. The mechanism of adenosine triphosphate depletion in the liver after a load of fructose. A kinetic study of liver adenylate deaminase. Biochem J 1977; 162: 601-609.
16. Cirillo P, Gersch MS, Mu W, Scherer PM, Kim KM, Gesualdo L, et al. Ketohexokinase-dependent metabolism of fructose induces proinflammatory mediators in proximal tubular cells. J Am Soc Nephrol 2009; 20: 545-553.
17. Glushakova O, Kosugi T, Roncal C, Mu W, Heinig M, Cirillo P, et al. Fructose induces the inflammatory molecule ICAM-1 in endothelial cells. J Am Soc Nephrol 2008; 19: 1712-1720.
18. Cortez-Pinto H, Chatham J, Chacko VP, Arnold C, Rashid A, Diehl AM. Alterations in liver ATP homeostasis in human nonalcoholic steatohepatitis: a pilot study. JAMA 1999; 282: 1659-1664.
19. Nair S, P Chacko V, Arnold C, Diehl AM. Hepatic ATP reserve and efficiency of replenishing: comparison between obese and nonobese normal individuals. Am J Gastroenterol 2003; 98: 466-470.
20. Bode JC, Zelder O, Rumpelt HJ, Wittkamp U. Depletion of liver adenosine phosphates and metabolic effects of intravenous infusion of fructose or sorbitol in man and in the rat. Eur J Clin Invest 1973; 3: 436-441.
21. Parks EJ, Skokan LE, Timlin MT, Dingfelder CS. Dietary sugars stimulate fatty acid synthesis in adults. J Nutr 2008; 138: 1039-1046.
22. Rashid A, Wu TC, Huang CC, Chen CH, Lin HZ, Yang SQ, et al. Mitochondrial proteins that regulate apoptosis and necrosis are induced in mouse fatty liver. HEPATOLOGY 1999; 29: 1131-1138.
23. Aguirre V, Uchida T, Yenush L, Davis R, White MF. The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J Biol Chem 2000; 275: 9047-9054.
24. Chavin KD, Yang S, Lin HZ, Chatham J, Chacko VP, Hoek JB, et al. Obesity induces expression of uncoupling protein-2 in hepatocytes and promotes liver ATP depletion. J Biol Chem 1999; 274: 5692-5700.
25. Johnson RJ, Perez-Pozo SE, Sautin YY, Manitius J, Sanchez-Lozada LG, Feig DI, et al. Hypothesis: could excessive fructose intake and uric acid cause type 2 diabetes? Endocr Rev 2009; 30: 96-116.
26. Stirpe F, Della Corte E, Bonetti E, Abbondanza A, Abbati A, De Stefano F. Fructose-induced hyperuricaemia. Lancet 1970; 2: 1310-1311.
27. Li Y, Xu C, Yu C, Xu L, Miao M. Association of serum uric acid level with non-alcoholic fatty liver disease: a cross-sectional study. J Hepatol 2009; 50: 1029-1034.
28. Petta S, Camma C, Cabibi D, Di Marco V, Craxi A. Hyperuricemia is associated with histological liver damage in patients with non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2011; 34: 757-766.
29. Afzali A, Weiss NS, Boyko EJ, Ioannou GN. Association between serum uric acid level and chronic liver disease in the United States. HEPATOLOGY 2010; 52: 578-589.
30. Korieh A, Crouzoulon G. Dietary regulation of fructose metabolism in the intestine and in the liver of the rat. Duration of the effects of a high fructose diet after the return to the standard diet. Arch Int Physiol Biochim Biophys 1991; 99: 455-460.
31. Ryan DH, Espeland MA, Foster GD, Haffner SM, Hubbard VS, Johnson KC, et al. Look AHEAD (Action for Health in Diabetes): design and methods for a clinical trial of weight loss for the prevention of cardiovascular disease in type 2 diabetes. Control Clin Trials 2003; 24: 610-628.
32. Skinner HA, Sheu WJ. Reliability of alcohol use indices. The Lifetime Drinking History and the MAST. J Stud Alcohol 1982; 43: 1157-1170.
33. Vitolins MZ, Anderson AM, Delahanty L, Raynor H, Miller GD, Mobley C, et al. Action for Health in Diabetes (Look AHEAD) trial: baseline evaluation of selected nutrients and food group intake. J Am Diet Assoc 2009; 109: 1367-1375.
34. Solga SF, Horska A, Hemker S, Crawford S, Diggs C, Diehl AM, et al. Hepatic fat and adenosine triphosphate measurement in overweight and obese adults using 1H and 31P magnetic resonance spectroscopy. Liver Int 2008; 28: 675-681.
35. Gabr RE, Ouwerkerk R, Bottomley PA. Quantifying in vivo MR spectra with circles. J Magn Reson 2006; 179: 152-163.
36. Chmelik M, Schmid AI, Gruber S, Szendroedi J, Krssak M, Trattnig S, et al. Three-dimensional high-resolution magnetic resonance spectroscopic imaging for absolute quantification of 31P metabolites in human liver. Magn Reson Med 2008; 60: 796-802.
37. Gallis JL, Delmas-Beauvieux MC, Biran M, Rousse N, Durand T, Canioni P. Is cellular integrity responsible for the partial NMR invisibility of ATP in isolated ischemic rat liver? NMR Biomed 1991; 4: 279-285.
38. Meyerhoff DJ, Boska MD, Thomas AM, Weiner MW. Alcoholic liver disease: quantitative image-guided P-31 MR spectroscopy. Radiology 1989; 173: 393-400.
39. Rajanayagam V, Lee RR, Ackerman Z, Bradley WG, Ross BD. Quantitative P-31 MR spectroscopy of the liver in alcoholic cirrhosis. J Magn Reson Imaging 1992; 2: 183-190.
40. Szendroedi J, Chmelik M, Schmid AI, Nowotny P, Brehm A, Krssak M, et al. Abnormal hepatic energy homeostasis in type 2 diabetes. HEPATOLOGY 2009; 50: 1079-1086.
41. Caldwell SH, de Freitas LA, Park SH, Moreno ML, Redick JA, Davis CA, et al. Intramitochondrial crystalline inclusions in nonalcoholic steatohepatitis. HEPATOLOGY 2009; 49: 1888-1895.
42. Van den Berghe G. Fructose: metabolism and short-term effects on carbohydrate and purine metabolic pathways. Prog Biochem Pharmacol 1986; 21: 1-32.
43. Budillon G, Citarella C, Loguercio C, Nardone G, Sicolo P, Del Vecchio Blanco C. Hyperuricemia induced by fructose load in liver cirrhosis. Ital J Gastroenterol 1992; 24: 373-377.