Hyperuricemia and nonalcoholic fatty liver disease: from bedside to bench and back

Hepatology International

Volumn 10, Issue 2, 2016, Pages 286-293

  Xu, Chengfu ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Non alcoholic fatty liver disease; Uric acid; Xanthine oxidoreductase

Indexed keywords

ALLOPURINOL; BENZBROMARONE; FEBUXOSTAT; URIC ACID;

DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; GENETIC POLYMORPHISM; HUMAN; HYPERURICEMIA; INSULIN RESISTANCE; METABOLIC SYNDROME X; MORBIDITY; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PREVALENCE; PRIORITY JOURNAL; PROGNOSIS; REVIEW; ANIMAL; CROSS-SECTIONAL STUDY; METABOLISM; PROSPECTIVE STUDY;

ANIMALS; CROSS-SECTIONAL STUDIES; HUMANS; HYPERURICEMIA; NON-ALCOHOLIC FATTY LIVER DISEASE; PREVALENCE; PROGNOSIS; PROSPECTIVE STUDIES; URIC ACID;

EID: 84959514745     PISSN: 19360533     EISSN: 19360541     Source Type: Journal    
DOI: 10.1007/s12072-015-9682-5     Document Type: Review

References (74)

1. Boss GR, Seegmiller JE. Hyperuricemia and gout. Classification, complications and management. N Engl J Med 1979;300(26):1459–1468. doi:10.1056/nejm197906283002604
2. Grazia TM. Inborn errors in purine metabolism: role of 5′-nucleotidases and their involvement in the etiology of neurological impairments. Nucleosides Nucleotides Nucleic Acids 2011;30(12):1276–1283. doi:10.1080/15257770.2011.616869
3. Ho C, Miller K, Savaiano D, Crane R, Ericson K, Clifford A. Absorption and metabolism of orally administered purines in fed and fasted rats. J Nutr 1979;109:1377–1382
4. Bzowska A, Kulikowska E, Shugar D. Purine nucleoside phosphorylases: properties, functions, and clinical aspects. Pharmacol Ther 2000;88(3):349–425
5. Stirpe F, Della Corte E. The regulation of rat liver xanthine oxidase. Conversion in vitro of the enzyme activity from dehydrogenase (type D) to oxidase (type O). J Biol Chem 1969;244(14):3855–3863
6. Harrison R. Structure and function of xanthine oxidoreductase: Where are we now? Free Radic Biol Med 2002;33(6):774–797
7. Battelli MG, Bolognesi A, Polito L. Pathophysiology of circulating xanthine oxidoreductase: new emerging roles for a multi-tasking enzyme. Biochim Biophys Acta 2014;1842(9):1502–1517. doi:10.1016/j.bbadis.2014.05.022
8. Krenitsky TA, Neil SM, Elion GB, Hitchings GH. A comparison of the specificities of xanthine oxidase and aldehyde oxidase. Arch Biochem Biophys 1972;150(2):585–599
9. McCord JM, Fridovich I. The reduction of cytochrome c by milk xanthine oxidase. J Biol Chem 1968;243(21):5753–5760
10. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 1985;312(3):159–163. doi:10.1056/nejm198501173120305
11. Maesaka JK, Fishbane S. Regulation of renal urate excretion: a critical review. Am J Kidney Dis 1998;32(6):917–933
12. Eraly SA, Vallon V, Rieg T, Gangoiti JA, Wikoff WR, Siuzdak G, et al. Multiple organic anion transporters contribute to net renal excretion of uric acid. Physiol Genomics 2008;33(2):180–192. doi:10.1152/physiolgenomics.00207.2007
13. Caulfield MJ, Munroe PB, O’Neill D, Witkowska K, Charchar FJ, Doblado M, et al. SLC2A9 is a high-capacity urate transporter in humans. PLoS Med 2008;5(10):e197. doi:10.1371/journal.pmed.0050197
14. Sorensen L, Levinson D. Origin and extrarenal elimination of uric acid in man. Nephron 1975;14(1):7–20
15. Van den Berghe G. Fructose: metabolism and short-term effects on carbohydrate and purine metabolic pathways. Prog Biochem Pharmacol 1986;21:1–32
16. Lanaspa MA, Sanchez-Lozada LG, Cicerchi C, Li N, Roncal-Jimenez CA, Ishimoto T, et al. Uric acid stimulates fructokinase and accelerates fructose metabolism in the development of fatty liver. PLoS ONE 2012;7(10):e47948. doi:10.1371/journal.pone.0047948
17. Zhu Y, Pandya BJ, Choi HK. Prevalence of gout and hyperuricemia in the US general population: the National Health and Nutrition Examination Survey 2007–2008. Arthritis Rheum 2011;63(10):3136–3141. doi:10.1002/art.30520
18. Li C, Hsieh MC, Chang SJ. Metabolic syndrome, diabetes, and hyperuricemia. Curr Opin Rheumatol 2013;25(2):210–216. doi:10.1097/BOR.0b013e32835d951e
19. Lonardo A, Loria P, Leonardi F, Borsatti A, Neri P, Pulvirenti M, et al. Fasting insulin and uric acid levels but not indices of iron metabolism are independent predictors of non-alcoholic fatty liver disease. A case–control study. Dig Liver Dis 2002;34(3):204–211
20. Lee S, Jin Kim Y, Yong Jeon T, Hoi Kim H, Woo OhS, Park Y, et al. Obesity is the only independent factor associated with ultrasound-diagnosed non-alcoholic fatty liver disease: a cross-sectional case-control study. Scand J Gastroenterol 2006;41(5):566–572. doi:10.1080/00365520500319591
21. Baba T, Amasaki Y, Soda M, Hida A, Imaizumi M, Ichimaru S, et al. Fatty liver and uric acid levels predict incident coronary heart disease but not stroke among atomic bomb survivors in Nagasaki. Hypertens Res 2007;30(9):823–829. doi:10.1291/hypres.30.823
22. 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(5):1029–1034. doi:10.1016/j.jhep.2008.11.021
23. Cai W, Wu X, Zhang B, Miao L, Sun YP, Zou Y, et al. Serum uric acid levels and non-alcoholic fatty liver disease in Uyghur and Han ethnic groups in northwestern China. Arq Bras Endocrinol Metabol 2013;57(8):617–622
24. Cai W, Song JM, Zhang B, Sun YP, Yao H, Zhang YX. The prevalence of nonalcoholic fatty liver disease and relationship with serum uric acid level in Uyghur population. Scientific World Journal 2014;2014:393628. doi:10.1155/2014/393628
25. 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 2013;62(3):392–399. doi:10.1016/j.metabol.2012.08.013
26. Shih MH, Lazo M, Liu SH, Bonekamp S, Hernaez R, Clark JM. Association between serum uric acid and nonalcoholic fatty liver disease in the US population. J Formos Med Assoc 2015;114(4):314–320. doi:10.1016/j.jfma.2012.11.014
27. Keenan T, Blaha MJ, Nasir K, Silverman MG, Tota-Maharaj R, Carvalho JA, et al. Relation of uric acid to serum levels of high-sensitivity C-reactive protein, triglycerides, and high-density lipoprotein cholesterol and to hepatic steatosis. Am J Cardiol 2012;110(12):1787–1792. doi:10.1016/j.amjcard.2012.08.012
28. Zelber-Sagi S, Ben-Assuli O, Rabinowich L, Goldstein A, Magid A, Shalev V, et al. The association between the serum levels of uric acid and alanine aminotransferase in a population-based cohort. Liver Int 2015;35(11):2408–2415 doi:10.1111/liv.12842
29. Sogabe M, Okahisa T, Taniguchi T, Tomonari T, Tanaka T, Tanaka H, et al. Light alcohol consumption plays a protective role against non-alcoholic fatty liver disease in Japanese men with metabolic syndrome. Liver Int 2015;35(6):1707–1714. doi:10.1111/liv.12754
30. Sertoglu E, Ercin CN, Celebi G, Gurel H, Kayadibi H, Genc H, et al. The relationship of serum uric acid with non-alcoholic fatty liver disease. Clin Biochem 2014;47(6):383–388. doi:10.1016/j.clinbiochem.2014.01.029
31. Sesti G, Fiorentino TV, Arturi F, Perticone M, Sciacqua A, Perticone F. Association between noninvasive fibrosis markers and chronic kidney disease among adults with nonalcoholic fatty liver disease. PLoS ONE 2014;9(2):e88569. doi:10.1371/journal.pone.0088569
32. 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(7):757–766. doi:10.1111/j.1365-2036.2011.04788.x
33. Wu SJ, Zhu GQ, Ye BZ, Kong FQ, Zheng ZX, Zou H, et al. Association between sex-specific serum uric acid and non-alcoholic fatty liver disease in Chinese adults: a large population-based study. Medicine 2015;94(17):e802. doi:10.1097/md.0000000000000802
34. Hwang IC, Suh SY, Suh AR, Ahn HY. The relationship between normal serum uric acid and nonalcoholic fatty liver disease. J Korean Med Sci 2011;26(3):386–391. doi:10.3346/jkms.2011.26.3.386
35. Lee YJ, Lee HR, Lee JH, Shin YH, Shim JY. Association between serum uric acid and non-alcoholic fatty liver disease in Korean adults. Clin Chem Lab Med 2010;48(2):175–180. doi:10.1515/cclm.2010.037
36. Xie Y, Wang M, Zhang Y, Zhang S, Tan A, Gao Y, et al. Serum uric acid and non-alcoholic fatty liver disease in non-diabetic Chinese men. PLoS ONE 2013;8(7):e67152. doi:10.1371/journal.pone.0067152
37. Hardwick RN, Fisher CD, Canet MJ, Scheffer GL, Cherrington NJ. Variations in ATP-binding cassette transporter regulation during the progression of human nonalcoholic fatty liver disease. Drug Metab Dispos 2011;39(12):2395–2402. doi:10.1124/dmd.111.041012
38. Liang J, Pei Y, Gong Y, Liu XK, Dou LJ, Zou CY, et al. Serum uric acid and non-alcoholic fatty liver disease in non-hypertensive Chinese adults: the cardiometabolic risk in Chinese (CRC) study. Eur Rev Med Pharmacol Sci 2015;19(2):305–311
39. Wang Z, Xu M, Peng J, Jiang L, Hu Z, Wang H, et al. Prevalence and associated metabolic factors of fatty liver disease in the elderly. Exp Gerontol 2013;48(8):705–709. doi:10.1016/j.exger.2013.05.059
40. Liu P, Ma F, Lou H, Zhu Y, Chen Y. Relationship between normal serum uric acid levels and nonalcoholic fatty liver disease in postmenopausal women. Chin J Hepatol 2014;22(1):53–57. doi:10.3760/cma.j.issn.1007-3418.2014.01.012
41. Liu PJ, Ma F, Lou HP, Zhu YN, Chen Y. Relationship between serum uric acid levels and hepatic steatosis in non-obese postmenopausal women. Climacteric 2014;17(6):692–699. doi:10.3109/13697137.2014.926323
42. Moon SS. Relationship between serum uric acid level and nonalcoholic fatty liver disease in pre- and postmenopausal women. Ann Nutr Metab 2013;62(2):158–163. doi:10.1159/000346202
43. Sullivan JS, Le MT, Pan Z, Rivard C, Love-Osborne K, Robbins K, et al. Oral fructose absorption in obese children with non-alcoholic fatty liver disease. Pediatr Obes 2015;10(3):188–195. doi:10.1111/ijpo.238
44. Vos MB, Colvin R, Belt P, Molleston JP, Murray KF, Rosenthal P, et al. Correlation of vitamin E, uric acid, and diet composition with histologic features of pediatric NAFLD. J Pediatr Gastroenterol Nutr 2012;54(1):90–96. doi:10.1097/MPG.0b013e318229da1a
45. Cardoso AS, Gonzaga NC, Medeiros CC, Carvalho DF. Association of uric acid levels with components of metabolic syndrome and non-alcoholic fatty liver disease in overweight or obese children and adolescents. J Pediatr 2013;89(4):412–418. doi:10.1016/j.jped.2012.12.008
46. Xia MF, Lin HD, Li XM, Yan HM, Bian H, Chang XX, et al. Renal function-dependent association of serum uric acid with metabolic syndrome and hepatic fat content in a middle-aged and elderly Chinese population. Clin Exp Pharmacol Physiol 2012;39(11):930–937. doi:10.1111/1440-1681.12011
47. Xu C, Yu C, Xu L, Miao M, Li Y. High serum uric acid increases the risk for nonalcoholic Fatty liver disease: a prospective observational study. PLoS ONE 2010;5(7):e11578. doi:10.1371/journal.pone.0011578
48. Xu C, Yu C, Ma H, Xu L, Miao M, Li Y. Prevalence and risk factors for the development of nonalcoholic fatty liver disease in a nonobese Chinese population: the Zhejiang Zhenhai Study. Am J Gastroenterol 2013;108(8):1299–1304. doi:10.1038/ajg.2013.104
49. Ryu S, Chang Y, Kim SG, Cho J, Guallar E. Serum uric acid levels predict incident nonalcoholic fatty liver disease in healthy Korean men. Metabolism 2011;60(6):860–866. doi:10.1016/j.metabol.2010.08.005
50. Lee JW, Cho YK, Ryan M, Kim H, Lee SW, Chang E, et al. Serum uric acid as a predictor for the development of nonalcoholic fatty liver disease in apparently healthy subjects: a 5-year retrospective cohort study. Gut Liver 2010;4(3):378–383. doi:10.5009/gnl.2010.4.3.378
51. Xu C, Wan X, Xu L, Weng H, Yan M, Miao M, et al. Xanthine oxidase in non-alcoholic fatty liver disease and hyperuricemia: one stone hits two birds. J Hepatol 2015;62(6):1412–1419. doi:10.1016/j.jhep.2015.01.019
52. Ryu S, Chang Y, Zhang Y, Kim SG, Cho J, Son HJ, et al. A cohort study of hyperuricemia in middle-aged South Korean men. Am J Epidemiol 2012;175(2):133–143. doi:10.1093/aje/kwr291
53. Choi YJ, Shin HS, Choi HS, Park JW, Jo I, Oh ES, et al. Uric acid induces fat accumulation via generation of endoplasmic reticulum stress and SREBP-1c activation in hepatocytes. Lab Invest 2014;94(10):1114–1125. doi:10.1038/labinvest.2014.98
54. Ferre P, Foufelle F. Hepatic steatosis: a role for de novo lipogenesis and the transcription factor SREBP-1c. Diabetes Obes Metab 2010;12(Suppl 2):83–92. doi:10.1111/j.1463-1326.2010.01275.x
55. Li X, Huang W, Gu J, Du X, Lei L, Yuan X, et al. SREBP-1c overactivates ROS-mediated hepatic NF-kappaB inflammatory pathway in dairy cows with fatty liver. Cell Signal 2015;27(10):2099–2109. doi:10.1016/j.cellsig.2015.07.011
56. Lanaspa MA, Sanchez-Lozada LG, Choi YJ, Cicerchi C, Kanbay M, Roncal-Jimenez CA, et al. Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: potential role in fructose-dependent and -independent fatty liver. J Biol Chem 2012;287(48):40732–40744. doi:10.1074/jbc.M112.399899
57. Havel PJ. Dietary fructose: implications for dysregulation of energy homeostasis and lipid/carbohydrate metabolism. Nutr Rev 2005;63(5):133–157
58. O’Sullivan TA, Oddy WH, Bremner AP, Sherriff JL, Ayonrinde OT, Olynyk JK, et al. Lower fructose intake may help protect against development of nonalcoholic fatty liver in adolescents with obesity. J Pediatr Gastroenterol Nutr 2014;58(5):624–631. doi:10.1097/mpg.0000000000000267
59. Kanerva N, Sandboge S, Kaartinen NE, Mannisto S, Eriksson JG. Higher fructose intake is inversely associated with risk of nonalcoholic fatty liver disease in older Finnish adults. Am J Clin Nutr 2014;100(4):1133–1138. doi:10.3945/ajcn.114.086074
60. Lim JS, Mietus-Snyder M, Valente A, Schwarz JM, Lustig RH. The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome. Nat Rev Gastroenterol Hepatol 2010;7(5):251–264. doi:10.1038/nrgastro.2010.41
61. Ackerman Z, Oron-Herman M, Grozovski M, Rosenthal T, Pappo O, Link G, et al. Fructose-induced fatty liver disease: hepatic effects of blood pressure and plasma triglyceride reduction. Hypertension 2005;45(5):1012–1018. doi:10.1161/01.hyp.0000164570.20420.67
62. Modan M, Halkin H, Karasik A, Lusky A. Elevated serum uric acid—a facet of hyperinsulinaemia. Diabetologia 1987;30(9):713–718
63. Quinones Galvan A, Natali A, Baldi S, Frascerra S, Sanna G, Ciociaro D, et al. Effect of insulin on uric acid excretion in humans. Am J Physiol 1995;268(1):E1–E5
64. Perez-Ruiz F, Aniel-Quiroga MA, Herrero-Beites AM, Chinchilla SP, Erauskin GG, Merriman T. Renal clearance of uric acid is linked to insulin resistance and lower excretion of sodium in gout patients. Rheumatol Int 2015;35(9):1519–1524. doi:10.1007/s00296-015-3242-0
65. Zhu Y, Hu Y, Huang T, Zhang Y, Li Z, Luo C, et al. High uric acid directly inhibits insulin signalling and induces insulin resistance. Biochem Biophys Res Commun 2014;447(4):707–714. doi:10.1016/j.bbrc.2014.04.080
66. Brunt EM. Pathology of nonalcoholic fatty liver disease. Nat Rev Gastroenterol Hepatol 2010;7(4):195–203. doi:10.1038/nrgastro.2010.21
67. Zhang Y, Yamamoto T, Hisatome I, Li Y, Cheng W, Sun N, et al. Uric acid induces oxidative stress and growth inhibition by activating adenosine monophosphate-activated protein kinase and extracellular signal-regulated kinase signal pathways in pancreatic beta cells. Mol Cell Endocrinol 2013;375(1–2):89–96. doi:10.1016/j.mce.2013.04.027
68. Zhang JX, Zhang YP, Wu QN, Chen B. Uric acid induces oxidative stress via an activation of the renin-angiotensin system in 3T3-L1 adipocytes. Endocrine 2015;48(1):135–142. doi:10.1007/s12020-014-0239-5
69. Verzola D, Ratto E, Villaggio B, Parodi EL, Pontremoli R, Garibotto G, et al. Uric acid promotes apoptosis in human proximal tubule cells by oxidative stress and the activation of NADPH oxidase NOX 4. PLoS ONE 2014;9(12):e115210. doi:10.1371/journal.pone.0115210
70. Albano E, Mottaran E, Occhino G, Reale E, Vidali M. Review article: role of oxidative stress in the progression of non-alcoholic steatosis. Aliment Pharmacol Ther 2005;22(Suppl 2):71–73. doi:10.1111/j.1365-2036.2005.02601.x
71. Garcia-Ruiz I, Rodriguez-Juan C, Diaz-Sanjuan T, del Hoyo P, Colina F, Munoz-Yague T, et al. Uric acid and anti-TNF antibody improve mitochondrial dysfunction in ob/ob mice. Hepatology 2006;44(3):581–591. doi:10.1002/hep.21313
72. Hayden MR, Tyagi SC. Uric acid: a new look at an old risk marker for cardiovascular disease, metabolic syndrome, and type 2 diabetes mellitus: the urate redox shuttle. Nutr Metab 2004;1(1):10. doi:10.1186/1743-7075-1-10
73. Xu CF, Yu CH, Xu L, Sa XY, Li YM. Hypouricemic therapy: a novel potential therapeutic option for nonalcoholic fatty liver disease. Hepatology 2010;52(5):1865–1866. doi:10.1002/hep.23798
74. Nakatsu Y, Seno Y, Kushiyama A, Sakoda H, Fujishiro M, Katasako A, et al. The xanthine oxidase inhibitor febuxostat suppresses development of nonalcoholic steatohepatitis in a rodent model. Am J Physiol Gastrointest Liver Physiol 2015;309(1):G42–G51. doi:10.1152/ajpgi.00443.2014