The rate of production of uric acid by hepatocytes is a sensitive index of compromised cell ATP homeostasis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 10, 2013, Pages

  Petrie, John L ^a   Patman, Gillian L ^a   Sinha, Ishita ^a   Alexander, Thomas D ^a   Reeves, Helen L ^a   Agius, Loranne ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Fructose; Hyperuricemia; Mitochondrial function; Nonalcoholic fatty liver disease

Indexed keywords

ADENINE NUCLEOTIDE; ADENOSINE; ADENOSINE MONOPHOSPHATE DEAMINASE; ADENOSINE TRIPHOSPHATE; FRUCTOSE; GLUCAGON; GLYCEROL; GLYCEROPHOSPHATE; INOSINE; INSULIN; PHOSPHATE; PHOSPHATE TRANSPORTER; ROTENONE; URIC ACID; XANTHINE;

ALCOHOL CONSUMPTION; ANIMAL CELL; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; DEGRADATION; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN CELL; LIVER BIOPSY; LIVER CELL; MALE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; URIC ACID BLOOD LEVEL;

FRUCTOSE; HYPERURICEMIA; MITOCHONDRIAL FUNCTION; NONALCOHOLIC FATTY LIVER DISEASE;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOLOGICAL MARKERS; CELLS, CULTURED; HEALTH STATUS INDICATORS; HEP G2 CELLS; HEPATOCYTES; HOMEOSTASIS; HUMANS; MALE; METABOLIC DISEASES; MICE; MICE, INBRED C3H; RATS; RATS, WISTAR; SENSITIVITY AND SPECIFICITY; URIC ACID;

EID: 84887591021     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00214.2013     Document Type: Article

References (44)

1. Abdelmalek MF, Lazo M, Horska A, Bonekamp S, Lipkin EW, Balasubramanyam A, Bantle JP, Johnson RJ, Diehl AM, Clark JM. Fatty Liver Subgroup of Look AHEAD Research Group. Higher dietary fructose is associated with impaired hepatic adenosine triphosphate ho-meostasis in obese individuals with type 2 diabetes. Hepatology 56: 952-960, 2012.
2. Afzali A, Weiss NS, Boyko EJ, Ioannou GN. Association between serum uric acid level and chronic liver disease in the United States. Hepatology 52: 578-589, 2010.
3. Agius L. High-carbohydrate diets induce hepatic insulin resistance to protect the liver from substrate overload. Biochem Pharmacol 85: 306- 312, 2012.
4. Arch JR, Newsholme EA. Activities and some properties of 5=-nucleoti-dase, adenosine kinase and adenosine deaminase in tissues from vertebrates and invertebrates in relation to the control of the concentration and the physiological role of adenosine. Biochem J 174: 965-977, 1978.
5. Arden C, Petrie JL, Tudhope SJ, Al-Oanzi Z, Claydon AJ, Beynon RJ, Towle HC, Agius L. Elevated glucose represses liver glucokinase and induces its regulatory protein to safeguard hepatic phosphate homeostasis. Diabetes 60: 3110-3120, 2011.
6. Arden C, Tudhope SJ, Petrie JL, Al-Oanzi ZH, Cullen KS, Lange AJ, Towle HC, Agius L. Fructose 2,6-bisphosphate is essential for glucose-regulated gene transcription of glucose-6-phosphatase and other ChREBP target genes in hepatocytes. Biochem J 443: 111-123, 2012.
7. Bontemps F, Van den Berghe G, Hers HG. Evidence for a substrate cycle between AMP and adenosine in isolated hepatocytes. Proc Natl Acad Sci USA 80: 2829-2833, 1983.
8. Brunt EM, Kleiner DE, Wilson LA, Belt P, Neuschwander-Tetri BA. NASH Clinical Research Network (CRN). Nonalcoholic fatty liver disease (NAFLD) activity score and the histopathologic diagnosis in NAFLD: distinct clinicopathologic meanings Hepatology 53: 810-820, 2011.
9. Burgess SC, Iizuka K, Jeoung NH, Harris RA, Kashiwaya Y, Veech RL, Kitazume T, Uyeda K. Carbohydrate-response element-binding protein deletion alters substrate utilization producing an energy-deficient liver. J Biol Chem 283: 1670-1678, 2008.
10. Cortez-Pinto H, Chatham J, Chacko VP, Arnold C, Rashid A, Diehl AM. Alterations in liver ATP homeostasis in human nonalcoholic steato-hepatitis: a pilot study. J Am Med Assoc 282: 1659-1664, 1999.
11. Cunningham CC, Malloy CR, Radda GK. Effect of fasting and acute ethanol administration on the energy state of in vivo liver as measured by 31P-NMR spectroscopy. Biochim Biophys Acta 885: 12-22, 1986.
12. de Groot H, de Groot H, Noll T. Enzymic determination of inorganic phosphates, organic phosphates and phosphate-liberating enzymes by use of nucleoside phosphorylase-xanthine oxidase (dehydrogenase)-coupled reactions. Biochem J 230: 255-260, 1985.
13. Faller J, Fox IH. Ethanol-induced hyperuricemia: evidence for increased urate production by activation of adenine nucleotide turnover. N Engl J Med 307: 1598-1602, 1982.
14. Grunst J, Dietze G, Wicklmayr M. Effect of ethanol on uric acid production of human liver. Nutr Metab 21, Suppl 1: 138-141, 1977.
15. Grunst J, Dietze G, Wicklmayr M, Hoppe F, Mehnert H. Influence of parenteral fructose or glucose administration on uric acid formation and phosphate uptake of the human liver. Z Ernahrungswiss 14: 259-267, 1975.
16. Hampp R. Adenosine 5=-diphosphate, and adenosine 5=-monophosphate Luminometri Method. In: Methods of Enzymatic Analysis, edited by Bergmeyer HU. vol. VII, 1985, p. 370-379.
17. Holdsworth CD, Dawson AM. Absorption of fructose in man. Proc Soc Exp Biol Med 118: 142-145, 1965.
18. Kolz Johnson T M, Sanna S, Teumer A, Vitart V, Perola M. Meta-analysis of 28,141 individuals identifies common variants within five new loci that influence uric acid concentrations. PLoS Genet 5: e1000504, 2009.
19. Köttgen A, Albrecht E, Teumer A, Vitart V, Krumsiek J. Genome-wide association analyses identify 18 new loci associated with serum urate concentrations. Nat Genet 45: 145-54, 2013.
20. 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 50: 1029-1034, 2009.
21. Masson S, Henriksen O, Stengaard A, Thomsen C, Quistorff B. Hepatic metabolism during constant infusion of fructose; comparative studies with 31P-magnetic resonance spectroscopy in man and rats. Biochim Biophys Acta 1199: 166-174, 1994.
22. Mayes PA. Intermediary metabolism of fructose. Am J Clin Nutr 58: 754S-765S, 1993.
23. Perheentupa J, Raivio K. Fructose-induced hyperuricaemia. Lancet 2: 528-531, 1967.
24. Puig JG, Fox IH. Ethanol-induced activation of adenine nucleotide turnover. Evidence for a role of acetate. J Clin Invest 74: 936-941, 1984.
25. Püschel GP, Nath A, Jungermann K. Increase of urate formation by stimulation of sympathetic hepatic nerves, circulating noradrenaline and glucagon in the perfused rat liver. FEBS Lett 219: 145-150, 1987.
26. Santoro N, Zhang CK, Zhao H, Pakstis AJ, Kim G, Kursawe R. Variant in the glucokinase regulatory protein (GCKR) gene is associated with fatty liver in obese children and adolescents. Hepatology 55: 781-789, 2012.
27. Sestoft L, Kristensen LO. Determination of unidirectional fluxes of phosphate across plasma membrane in isolated perfused rat liver. Am J Physiol Cell Physiol 236: C202-C210, 1979.
28. Sirota JC, McFann K, Targher G, Johnson RJ, Chonchol M, Jalal DI. Elevated serum uric acid levels are associated with non-alcoholic fatty liver disease independently of metabolic syndrome features in the United States: Liver ultrasound data from the National Health and Nutrition Examination Survey. Metabolism 62: 392-399, 2013.
29. So A, Thorens B. Uric acid transport and disease. J Clin Invest 120: 1791-1799, 2010.
30. Son N, Hur HJ, Sung MJ, Kim MS, Hwang JT, Park JH, Yang HJ, Kwon DY, Yoon Chung HY SH, Kim HJ. Liquid chromatography-mass spectrometry-based metabolomic analysis of livers from aged rats. J Proteome Res 11: 2251-2258, 2012.
31. Speliotes EK, Yerges-Armstrong LM, Wu J, Hernaez R, Kim LJ, Palmer CD, Consortium GOLD. Genome-wide association analysis identifies variants associated with nonalcoholic fatty liver disease that have distinct effects on metabolic traits. PLoS Genet 7: e1001324, 2011.
32. Szendroedi J, Chmelik M, Schmid AI, Nowotny P, Brehm A, Krssak M, Moser E, Roden M. Abnormal hepatic energy homeostasis in type 2 diabetes. Hepatology 50: 1079-1086, 2009.
33. Tappy L, Mittendorfer B. Fructose toxicity: is the science ready for public health actions? Curr Opin Clin Nutr Metab Care 15: 357-361, 2012.
34. Van den Berghe G. Inborn errors of fructose metabolism. Annu Rev Nutr 14: 41-58, 1994.
35. Van den Berghe G, Bontemps F, Hers HG. Purine catabolism in isolated rat hepatocytes. Influence of coformycin. Biochem J 188: 913-920, 1980.
36. 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 162: 601-609, 1977.
37. Veech RL, Guynn R, Veloso D. The time-course of the effects of ethanol on the redox and phosphorylation states of rat liver. Biochem J 127: 387-397, 1972.
38. Vukovic J, Modun D, Budimir D, Sutlovic D, Salamunic I, Zaja I, Boban M. Acute, food-induced moderate elevation of plasma uric acid protects against hyperoxia-induced oxidative stress and increase in arterial stiffness in healthy humans. Atherosclerosis 207: 255-260, 2009.
39. Vuorinen-Markkola H, Yki-Järvinen H. Hyperuricemia and insulin resistance. J Clin Endocrinol Metab 78: 25-29, 1994.
40. Wang DD, Sievenpiper JL, de Souza RJ, Chiavaroli L, Ha V, Cozma AI, Mirrahimi A, Yu ME, Carleton AJ, Di Buono M, Jenkins AL, Leiter LA, Wolever TM, Beyene J, Kendall CW, Jenkins DJ. The effects of fructose intake on serum uric acid vary among controlled dietary trials. J Nutr 142: 916-923, 2012.
41. Wright AF, Rudan I, Hastie ND, Campbell H. A 'complexity' of urate transporters. Kidney Int 78: 446-452, 2010.
42. Wyngaarden JB. Overproduction of uric acid as the cause of hyperuri-cemia in primary gout. J Clin Invest 36: 1508-1515, 1957.
43. Yamamoto T, Moriwaki Y, Takahashi S. Effect of ethanol on metabolism of purine bases (hypoxanthine, xanthine, and uric acid). Clin Chim Acta 356: 35-57, 2005.
44. Yang Q, Köttgen A, Dehghan A, Smith AV, Glazer NL. Multiple genetic loci influence serum urate levels and their relationship with gout and cardiovascular disease risk factors. Circ Cardiovasc Genet 3: 523-530, 2010.