Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: Potential role in fructose-dependent and -independent fatty liver

Journal of Biological Chemistry

Volumn 287, Issue 48, 2012, Pages 40732-40744

  Lanaspa, Miguel A ^a   Sanchez Lozada, Laura G ^a,b   Choi, Yea Jin ^c   Cicerchi, Christina ^a   Kanbay, Mehmet ^d   Roncal Jimenez, Carlos A ^a   Ishimoto, Takuji ^a   Li, Nanxing ^a   Marek, George ^e   Duranay, Murat ^d   Schreiner, George ^f   Rodriguez Iturbe, Bernardo ^g   Nakagawa, Takahiko ^a   Kang, Duk Hee ^c   Sautin, Yuri Y ^e   Johnson, Richard J ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b INSTITUTO NACIONAL DE CARDIOLOGÍA IGNACIO CHÁVEZ   (Mexico)

^c Ewha Womans University School of Medicine   (South Korea)

^d Division of Nephrology Kayseri Training and Research Hospital   (Turkey)

^e UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^f Cardero Therapeutics Incorporated   (United States)

^g UNIVERSIDAD DEL ZULIA   (Venezuela)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITASE; ATP-CITRATE LYASE; DEGRADATION PATHWAYS; FAT ACCUMULATION; FATTY LIVER; FRUCTOKINASE; HEALTH CONCERNS; HEPATIC STEATOSIS; KREBS CYCLE; METABOLIC SYNDROMES; MITOCHONDRIAL OXIDANTS; NON-ALCOHOLIC FATTY LIVER DISEASE; SOFT DRINKS; SYNTHASES; URIC ACIDS;

BEVERAGES; ENZYME ACTIVITY; FATTY ACIDS; METABOLISM; ORGANIC ACIDS; PHOSPHORYLATION;

FRUCTOSE;

ACONITATE HYDRATASE; ADENOSINE MONOPHOSPHATE DEAMINASE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE CITRATE LYASE; FATTY ACID SYNTHASE; FRUCTOKINASE; FRUCTOSE; PURINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRIACYLGLYCEROL; URIC ACID;

ADULT; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FATTY LIVER; FEMALE; HUMAN; HUMAN CELL; LIPID STORAGE; LIPOGENESIS; LIVER CELL; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; NONALCOHOLIC FATTY LIVER; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RISK FACTOR;

FATTY LIVER; FRUCTOSE; HEP G2 CELLS; HUMANS; LIPOGENESIS; MITOCHONDRIA; OXIDATIVE STRESS; TRIGLYCERIDES; URIC ACID;

ANIMALIA;

EID: 84869996114     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.399899     Document Type: Article

References (54)

1. Adams, L. A., Lymp, J. F., St Sauver, J., Sanderson, S. O., Lindor, K. D., Feldstein, A., and Angulo, P. (2005) The natural history of nonalcoholic fatty liver disease. A population-based cohort study. Gastroenterology 129, 113-121 (Pubitemid 41002048)
2. 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 nonalcoholic fatty liver disease. J. Hepatol. 48, 993-999
3. Lim, J. S., Mietus-Snyder, M., Valente, A., Schwarz, J. M., and Lustig, R. H. (2010) The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome. Nat. Rev. Gastroenterol. Hepatol. 7, 251-264
4. Abdelmalek, M. F., Lazo, M., Horska, A., Bonekamp, S., Lipkin, E. W., Balasubramanyan, A., Bantle, J. P., Johnson, R. J., Diehl, A. M., and Clark, J. M. (2012) Higher dietary fructose is associated with impaired hepatic ATP homeostasis in patients with nonalcoholic fatty liver disease. Hepatology 56, 952-960
5. Abdelmalek, M. F., Suzuki, A., Guy, C., Johnson, R. J., and Diehl, A. M. (2007) Fructose-induced hyperuricemia as a causal mechanism for nonalcoholic fatty liver disease. Hepatology 46, 293A (Abstr. 128)
6. Havel, P. J. (2005) Dietary fructose: implications for dysregulation of energy homeostasis and lipid/carbohydrate metabolism. Nutr. Rev. 63, 133-157
7. Ackerman, Z., Oron-Herman, M., Grozovski, M., Rosenthal, T., Pappo, O., Link, G., and Sela, B. A. (2005) Fructose-induced fatty liver disease. Hepatic effects of blood pressure and plasma triglyceride reduction. Hypertension 45, 1012-1018 (Pubitemid 40628952)
8. van den Berghe, G., Bronfman, M., Vanneste, R., and Hers, H. G. (1977) 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 (Pubitemid 8060796)
9. Perheentupa, J., and Raivio, K. (1967) Fructose-induced hyperuricaemia. Lancet 2, 528-531
10. Reiser, S., Powell, A. S., Scholfield, D. J., Panda, P., Ellwood, K. C., and Canary, J. J. (1989) Blood lipids, lipoproteins, apoproteins, and uric acid in men fed diets containing fructose or high amylose cornstarch. Am. J. Clin. Nutr. 49, 832-839 (Pubitemid 19139785)
11. Cox, C. L., Stanhope, K. L., Schwarz, J. M., Graham, J. L., Hatcher, B., Griffen, S. C., Bremer, A. A., Berglund, L., McGahan, J. P., Keim, N. L., and Havel, P. J. (2012) Consumption of fructose- but not glucose-sweetened beverages for 10 weeks increases circulating concentrations of uric acid, retinol-binding protein-4, and γ-glutamyl transferase activity in overweight/obese humans. Nutr. Metab. (Lond) 24, 68
12. Choi, J. W., Ford, E. S., Gao, X., and Choi, H. K. (2008) Sugar-sweetened soft drinks, diet soft drinks, and serum uric acid level. The third national health and nutrition examination survey. Arthritis Rheum. 59, 109-116 (Pubitemid 351171885)
13. Xu, C., Yu, C., Xu, L., Miao, M., and Li, Y. (2010) High serum uric acid increases the risk for nonalcoholic fatty liver disease. A prospective observational study. PLoS ONE 5, e11578
14. Kuo, C. F., Yu, K. H., Luo, S. F., Chiu, C. T., Ko, Y. S., Hwang, J. S., Tseng, W. Y., Chang, H. C., Chen, H. W., and See, L. C. (2010) Gout and risk of nonalcoholic fatty liver disease. Scand. J. Rheumatol. 39, 466-471
15. Li, Y., Xu, C., Yu, C., Xu, L., and Miao, M. (2009) Association of serum uric acid level with nonalcoholic fatty liver disease. A cross-sectional study. J. Hepatol. 50, 1029-1034
16. Lee, K. (2009) Relationship between uric acid and hepatic steatosis among Koreans. Diabetes Metab. 35, 447-451
17. Yamada, T., Suzuki, S., Fukatsu, M., Wada, T., Yoshida, T., and Joh, T. (2010) Elevated serum uric acid is an independent risk factor for nonalcoholic fatty liver disease in Japanese undergoing a health checkup. Acta Gastroenterol. Belg 73, 12-17
18. Petta, S., Cammà, C., Cabibi, D., Di Marco, V., and Craxì, A. (2011) Hyperuricemia is associated with histological liver damage in patients with nonalcoholic fatty liver disease. Aliment. Pharmacol. Ther. 34, 757-766
19. Lee, J. W., Cho, Y. K., Ryan, M., Kim, H., Lee, S. W., Chang, E., Joo, K. J., Kim, J. T., Kim, B. S., and Sung, K. C. (2010) 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 4, 378-383
20. Lonardo, A., Loria, P., Leonardi, F., Borsatti, A., Neri, P., Pulvirenti, M., Verrone, A. M., Bagni, A., Bertolotti, M., Ganazzi, D., and Carulli, N. (2002) Fasting insulin and uric acid levels but not indices of iron metabolism are independent predictors of nonalcoholic fatty liver disease. A case-control study. Dig. Liver Dis. 34, 204-211 (Pubitemid 34269566)
21. Ryu, S., Chang, Y., Kim, S. G., Cho, J., and Guallar, E. (2011) Serum uric acid levels predict incident nonalcoholic fatty liver disease in healthy Korean men. Metab. Clin. Exp. 60, 860-866
22. Sirota, J. C., McFann, K., Targher, G., Johnson, R. J., Chonchol, M., and Jalal, D. (2012) Association between serum uric acid levels and ultrasound-diagnosed nonalcoholic fatty liver disease in the National Health and Nutrition Examination Survey. Metabolism S0026-0495(12)0031 7-4
23. Xu, C. F., Yu, C. H., Xu, L., Sa, X. Y., and Li, Y. M. (2010) Hypouricemic therapy. A novel potential therapeutic option for nonalcoholic fatty liver disease. Hepatology 52, 1865-1866
24. Sautin, Y. Y., Nakagawa, T., Zharikov, S., and Johnson, R. J. (2007) Adverse effects of the classic antioxidant uric acid in adipocytes. NADPH oxidase-mediated oxidative/nitrosative stress. Am. J. Physiol. Cell Physiol 293, C584-C596 (Pubitemid 47235197)
25. Yu, M. A., Sánchez-Lozada, L. G., Johnson, R. J., and Kang, D. H. (2010) Oxidative stress with an activation of the renin-angiotensin system in human vascular endothelial cells as a novel mechanism of uric acid-induced endothelial dysfunction. J. Hypertens. 28, 1234-1242
26. Kang, D. H., Park, S. K., Lee, I. K., and Johnson, R. J. (2005) Uric acid-induced C-reactive protein expression. Implication on cell proliferation and nitric oxide production of human vascular cells. J. Am. Soc. Nephrol. 16, 3553-3562
27. Kanellis, J., Watanabe, S., Li, J. H., Kang, D. H., Li, P., Nakagawa, T., Wamsley, A., Sheikh-Hamad, D., Lan, H. Y., Feng, L., and Johnson, R. J. (2003) Uric acid stimulates monocyte chemoattractant protein-1 production in vascular smooth muscle cells via mitogen-activated protein kinase and cyclooxygenase-2. Hypertension 41, 1287-1293 (Pubitemid 36706079)
28. Corry, D. B., Eslami, P., Yamamoto, K., Nyby, M. D., Makino, H., and Tuck, M. L. (2008) Uric acid stimulates vascular smooth muscle cell proliferation and oxidative stress via the vascular renin-angiotensin system. J. Hypertens. 26, 269-275
29. Baldini, P. M., De Vito, P., Antenucci, D., Vismara, D., D'Aquilio, F., Luly, P., Zalfa, F., Bagni, C., and Di Nardo, P. (2004) Atrial natriuretic peptide induces cell death in human hepatoblastoma (HepG2) through the involvement of NADPH oxidase. Cell Death Differ. 11, S210-S212
30. Chaney, A. L., and Marbach, E. P. (1962) Modified reagents for determination of urea and ammonia. Clin. Chem. 8, 130-132
31. Block, K., Gorin, Y., and Abboud, H. E. (2009) Subcellular localization of Nox4 and regulation in diabetes. Proc. Natl. Acad. Sci. U.S.A. 106, 14385-14390
32. Baldwin, W., McRae, S., Marek, G., Wymer, D., Pannu, V., Baylis, C., Johnson, R. J., and Sautin, Y. Y. (2011) Hyperuricemia as a mediator of the proinflammatory endocrine imbalance in the adipose tissue in a murine model of the metabolic syndrome. Diabetes 60, 1258-1269
33. Cirillo, P., Gersch, M. S., Mu, W., Scherer, P. M., Kim, K. M., Gesualdo, L., Henderson, G. N., Johnson, R. J., and Sautin, Y. Y. (2009) Ketohexokinase-dependent metabolism of fructose induces proinflammatory mediators in proximal tubular cells. J. Am. Soc. Nephrol. 20, 545-553
34. Hausladen, A., and Fridovich, I. (1994) Superoxide and peroxynitrite inactivate aconitases but nitric oxide does not. J. Biol. Chem. 269, 29405-29408 (Pubitemid 24365084)
35. Deleted in proof
36. Johnson, R. J., Perez-Pozo, S. E., Sautin, Y. Y., Manitius, J., Sanchez-Lozada, L. G., Feig, D. I., Shafiu, M., Segal, M., Glassock, R. J., Shimada, M., Roncal, C., and Nakagawa, T. (2009) Hypothesis. Could excessive fructose intake and uric acid cause type 2 diabetes? Endocr. Rev. 30, 96-116
37. Tappy, L., and Lê, K. A. (2010) Metabolic effects of fructose and the worldwide increase in obesity. Physiol. Rev. 90, 23-46
38. Roncal-Jimenez, C. A., Lanaspa, M. A., Rivard, C. J., Nakagawa, T., Sanchez-Lozada, L. G., Jalal, D., Andres-Hernando, A., Tanabe, K., Madero, M., Li, N., Cicerchi, C., Mc Fann, K., Sautin, Y. Y., and Johnson, R. J. (2011) Sucrose induces fatty liver and pancreatic inflammation in male breeder rats independent of excess energy intake. Metab. Clin. Exp. 60, 1259-1270
39. Nikkilä, E. A. (1969) Control of plasma and liver triglyceride kinetics by carbohydrate metabolism and insulin. Adv. Lipid Res. 7, 63-134
40. Nikkilä, E. A., and Kekki, M. (1972) Effects of dietary fructose and sucrose on plasma triglyceride metabolism in patients with endogenous hypertriglyceridemia. Acta Med. Scand. Suppl. 542, 221-227
41. Van den Berghe, G. (1986) Fructose. Metabolism and short term effects on carbohydrate and purine metabolic pathways. Prog. Biochem. Pharmacol. 21, 1-32
42. Odièvre, M., Gentil, C., Gautier, M., and Alagille, D. (1978) Hereditary fructose intolerance in childhood. Diagnosis, management, and course in 55 patients. Am. J. Dis. Child. 132, 605-608 (Pubitemid 9125818)
43. Kodama, S., Saito, K., Yachi, Y., Asumi, M., Sugawara, A., Totsuka, K., Saito, A., and Sone, H. (2009) Association between serum uric acid and development of type 2 diabetes. Diabetes Care 32, 1737-1742
44. Masuo, K., Kawaguchi, H., Mikami, H., Ogihara, T., and Tuck, M. L. (2003) Serum uric acid and plasma norepinephrine concentrations predict subsequent weight gain and blood pressure elevation. Hypertension 42, 474-480 (Pubitemid 37237341)
45. Dehghan, A., van Hoek, M., Sijbrands, E. J., Hofman, A., and Witteman, J. C. (2008) High serum uric acid as a novel risk factor for type 2 diabetes. Diabetes Care 31, 361-362 (Pubitemid 351213351)
46. Nakagawa, T., Hu, H., Zharikov, S., Tuttle, K. R., Short, R. A., Glushakova, O., Ouyang, X., Feig, D. I., Block, E. R., Herrera-Acosta, J., Patel, J. M., and Johnson, R. J. (2006) A causal role for uric acid in fructose-induced metabolic syndrome. Am. J. Physiol. Renal Physiol. 290, F625-F631 (Pubitemid 43724964)
47. Feig, D. I., Soletsky, B., and Johnson, R. J. (2008) Effect of allopurinol on the blood pressure of adolescents with newly diagnosed essential hypertension: a randomized trial. JAMA 300, 922-930
48. Kanbay, M., Huddam, B., Azak, A., Solak, Y., Kadioglu, G. K., Kirbas, I., Duranay, M., Covic, A., and Johnson, R. J. (2011) A randomized study of allopurinol on endothelial function and estimated glomerular filtration rate in asymptomatic hyperuricemic subjects with normal renal function. Clin. J. Am. Soc. Nephrol. 6, 1887-1894
49. Ogino, K., Kato, M., Furuse, Y., Kinugasa, Y., Ishida, K., Osaki, S., Kinugawa, T., Igawa, O., Hisatome, I., Shigemasa, C., Anker, S. D., and Doehner, W. (2010) Uric acid-lowering treatment with benzbromarone in patients with heart failure. A double-blind placebo-controlled crossover preliminary study. Circ. Heart Fail. 3, 73-81
50. Kanbay, M., Ozkara, A., Selcoki, Y., Isik, B., Turgut, F., Bavbek, N., Uz, E., Akcay, A., Yigitoglu, R., and Covic, A. (2007) Effect of treatment of hyperuricemia with allopurinol on blood pressure, creatinine clearance, and proteinuria in patients with normal renal functions. Int. Urol. Nephrol. 39, 1227-1233 (Pubitemid 350193621)
51. Feig, D. I., Kang, D. H., and Johnson, R. J. (2008) Uric acid and cardiovascular risk. N. Engl. J. Med. 359, 1811-1821
52. Xu, P., LaVallee, P., and Hoidal, J. R. (2000) Repressed expression of the human xanthine oxidoreductase gene. E-box and TATA-like elements restrict ground state transcriptional activity. J. Biol. Chem. 275, 5918-5926 (Pubitemid 30115240)
53. Abdelmalak, M., Sukzuki, 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
54. Argalious, M. Y., Dalton, J. E., Cywinski, J. B., Seif, J., Abdelmalak, M., and Sessler, D. I. (2012) Association between preoperative statin therapy and postoperative change in glomerular filtration rate in endovascular aortic surgery. Br. J. Anaesth. 109, 161-167