Quercetin and allopurinol ameliorate kidney injury in STZ-treated rats with regulation of renal NLRP3 inflammasome activation and lipid accumulation

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Wang, Chuang ^a   Pan, Ying ^a   Zhang, Qing Yu ^a   Wang, Fu Meng ^a   Kong, Ling Dong ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPURINOL; APOPTOSIS ASSOCIATED SPECK LIKE PROTEIN; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; QUERCETIN; STREPTOZOCIN; UNCLASSIFIED DRUG; URATE; CELL RECEPTOR; CREATININE; NOD LIKE RECEPTOR 3, RAT; NOD-LIKE RECEPTOR 3, RAT; PRIMER DNA; URIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DYSLIPIDEMIA; HYPERURICEMIA; KIDNEY INJURY; LIPID METABOLISM; LIPID STORAGE; MALE; NEPHRITIS; NEPHROTOXICITY; NONHUMAN; PROTEIN SYNTHESIS INHIBITION; PROTEIN TRANSPORT; RAT; REGULATORY MECHANISM; ACUTE KIDNEY FAILURE; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; BODY WEIGHT; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; ORGAN SIZE; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; UREA NITROGEN BLOOD LEVEL; URINE; WESTERN BLOTTING;

ACUTE KIDNEY INJURY; ALLOPURINOL; ANALYSIS OF VARIANCE; ANIMALS; BLOOD UREA NITROGEN; BLOTTING, WESTERN; BODY WEIGHT; CREATININE; DIABETIC NEPHROPATHIES; DNA PRIMERS; GENE EXPRESSION REGULATION; INFLAMMASOMES; LIPID METABOLISM; MALE; ORGAN SIZE; QUERCETIN; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; STREPTOZOCIN; URIC ACID;

EID: 84862235344     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038285     Document Type: Article

References (66)

1. Ayodele OE, Alebiosu CO, Salako BL, (2004) Diabetic nephropathy-a review of the natural history, burden, risk factors and treatment. J Natl Med Assoc 96: 1445-1454.
2. Donath MY, Shoelson SE, (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11: 98-107.
3. Murea M, Freedman BI, Parks JS, Antinozzi PA, Elbein SC, et al. (2010) Lipotoxicity in diabetic nephropathy: the potential role of fatty acid oxidation. Clin J Am Soc Nephrol 5: 2373-2379.
4. Wellen KE, Hotamisligil GS, (2005) Inflammation, stress, and diabetes. J Clin Invest 115: 1111-1119.
5. Hovind P, Rossing P, Johnson RJ, Parving HH, (2011) Serum uric acid as a new player in the development of diabetic nephropathy. J Ren Nutr 21: 124-127.
6. Hovind P, Rossing P, Tarnow L, Johnson RJ, Parving HH, (2009) Serum uric acid as a predictor for development of diabetic nephropathy in type 1 diabetes: an inception cohort study. Diabetes 58: 1668-1671.
7. Gasse P, Riteau N, Charron S, Girre S, Fick L, et al. (2009) Uric acid is a danger signal activating NALP3 inflammasome in lung injury inflammation and fibrosis. Am J Respir Crit Care Med 179: 903-913.
8. Navarro-Gonzalez JF, Mora-Fernandez C, (2008) The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol 19: 433-442.
9. Dinarello CA, Donath MY, Mandrup-Poulsen T, (2010) Role of IL-1beta in type 2 diabetes. Curr Opin Endocrinol Diabetes Obes 17: 314-321.
10. Moriwaki YT, Yamamoto T, Shibutani Y, Aoki E, Tsutsumi Z, et al. (2003) Elevated levels of interleukin-18 and tumor necrosis factor-alpha in serum of patients with type 2 diabetes mellitus: relationship with diabetic nephropathy. Metabolism 52: 605-608.
11. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, et al. (2010) NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464: 1357-1361.
12. Rajamäki K, Lappalainen J, Oörni K, Valimaki E, Matikainen S, et al. (2010) Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS ONE 5: e11765.
13. Vilaysane A, Chun J, Seamone ME, Wang W, Chin R, et al. (2010) The NALP3 inflammasome promotes renal inflammation and contributes to CKD. J Am Soc Nephrol 21: 1732-1744.
14. Shigeoka AA, Mueller JL, Kambo A, Mathison JC, King AJ, et al. (2010) An inflammasome-independent role for epithelial-expressed Nlrp3 in renal ischemia-reperfusion injury. J Immunol 185: 6277-6285.
15. Masters SL, Dunne A, Subramanian SL, Hull RL, Tannahill GM, et al. (2010) Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol 11: 897-904.
16. Estevez EC, Priego MP, Barbudo JA, Guijo PS, (1990) Hyperuricemia-hyperlipemia association in the absence of obesity and alcohol abuse. Clin Rheumatol 9: 28-31.
17. Joosten LA, Netea MG, Mylona E, Koenders MI, Malireddi RKS, et al. (2010) Engagement of fatty acids with Toll-like receptor 2 drives interleukin-1β production via the ASC/caspase 1 pathway in monosodium urate monohydrate crystal-induced gouty arthritis. Arthritis Rheum 62: 3237-3248.
18. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, et al. (2011) The NALP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 17: 179-188.
19. Griffith JW, Sun T, McIntosh MT, Bucala R, (2009) Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol 183: 5208-5220.
20. Hu QH, Wang C, Li JM, Zhang DM, Kong LD, (2009) Allopurinol, rutin, and quercetin attenuate hyperuricemia and renal dysfunction in rats induced by fructose intake: renal organic ion transporter involvement. Am J Physiol Renal Physiol 297: F1080-F1091.
21. Reungjui S, Roncal CA, Mu W, Srinivas TR, Sirivongs D, et al. (2007) Thiazide diuretics exacerbate fructose-induced metabolic syndrome. J Am Soc Nephrol 18: 2724-2731.
22. Kosugi T, Nakayama T, Heinig M, Zhang L, Yuzawa Y, et al. (2009) Effect of lowering uric acid on renal disease in the type 2 diabetic db/db mice. Am J Physiol Renal Physiol 297: F481-488.
23. Momeni A, Shahidi S, Seirafian S, Taheri S, Kheiri S, (2010) Effect of allopurinol in decreasing proteinuria in type 2 diabetic patients. Iran J Kidney Dis 4: 128-132.
24. Rivera L, Moron R, Sanchez M, Zarzuelo A, Galisteo M, (2008) Quercetin ameliorates metabolic syndrome and improves the inflammatory status in obese Zucker rats. Obesity (Silver Spring) 16: 2081-2087.
25. Park J, Ahn J, Kim S, Ha TY, (2008) Quercetin suppresses the hyperlipidemia induced by an atherogenic diet in mice. FASEB J 22: lb707.
26. Chuang CC, Martinez K, Xie G, Kennedy A, Bumrungpert A, et al. (2010) Quercetin is equally or more effective than resveratrol in attenuating tumor necrosis factor-{alpha}-mediated inflammation and insulin resistance in primary human adipocytes. Am J Clin Nutr 92: 1511-1521.
27. Anjaneyulu M, Chopra K, (2004) Quercetin, an anti-oxidant bioflavonoid, attenuates diabetic nephropathy in rats. Clin Exp Pharmacol Physiol 31: 244-248.
28. Tone A, Shikata K, Sasaki M, Ohga S, Yozai K, et al. (2005) Erythromycin ameliorates renal injury via anti-inflammatory effects in experimental diabetic rats. Diabetologia 48: 2402-2411.
29. Abdel-Raheem IT, Abdel-Ghany AA, Mohamed GA, (2009) Protective effect of quercetin against gentamicin-induced nephrotoxicity in rats. Biol Pharm Bull 32: 61-67.
30. Edwards RL, Lyon T, Litwin SE, Rabovsky A, Symons JD, et al. (2007) Quercetin reduces blood pressure in hypertensive subjects. J Nutr 137: 2405-2411.
31. Mahesh T, Menon VP, (2004) Quercetin allievates oxidative stress in streptozotocin-induced diabetic rats. Phytother Res 18: 123-127.
32. Minami M, Ishiyama A, Takagi M, Omata M, Atarashi K, (2005) Effects of allopurinol, a xanthine oxidase inhibitor, on renal injury in hypercholesterolemia-induced hypertensive rats. Blood Press 14: 120-125.
33. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
34. Hediger MA, Johnson RJ, Miyazaki H, Endou H, (2005) Molecular physiology of urate transport. Physiology (Bethesda) 20: 125-133.
35. Guan Y, Breyer MD, (2001) Peroxisome proliferator-activated receptors (PPARs): novel therapeutic targets in renal disease. Kidney Int 60: 14-30.
36. Tamai I, Ohashi R, Nezu JI, Sai Y, Kobayashi D, et al. (2000) Molecular and functional characterization of organic cation/carnitine transporter family in mice. J Biol Chem 275: 40064-40072.
37. Krzystanek M, Pedersen TX, Bartels ED, Kjaehr J, Straarup EM, et al. (2010) Expression of apolipoprotein B in the kidney attenuates renal lipid accumulation. J Biol Chem 285: 10583-10590.
38. Kerner J, Hoppel C, (2000) Fatty acid import into mitochondria. Biochim Biophys Acta 1486: 1-17.
39. Wakil SJ, Abu-Elheiga LA, (2008) Fatty acid metabolism: target for metabolic syndrome. J Lipid Res 50 (Suppl): S138-S143.
40. Iyer SS, Pulskens WP, Sadler JJ, Butter LM, Teske GJ, et al. (2009) Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci USA 106: 20388-20393.
41. Keembiyehetty C, Augustin R, Carayannopoulos MO, Steer S, Manolescu A, et al, (2006) Mouse glucose transporter 9 splice variants are expressed in adult liver and kidney and are up-regulated in diabetes. Mol Endocrinol 20: 686-697.
42. Cheng QQ, Aleksunes LM, Manautou JE, Cherrington NJ, Scheffer GL, et al. (2008) Drug-metabolizing enzyme and transporter expression in a mouse model of diabetes and obesity. Mol Pharm 5: 77-91.
43. Wang Z, Jiang T, Li J, Proctor G, McManaman JL, et al. (2005) Regulation of renal lipid metabolism, lipid accumulation, and glomerulosclerosis in FVB db/db mice with type 2 diabetes. Diabetes 54: 2328-2335.
44. Hostetler HA, Huang H, Kier AB, Schroeder F, (2008) Glucose directly links to lipid metabolism through high affinity interaction with peroxisome proliferator-activated receptor alpha. J Biol Chem 283: 2246-2254.
45. Frigerio F, Brun T, Bartley C, Madsen L, Poulain P, et al. (2010) Peroxisome proliferator-activated receptor alpha (PPAR alpha) protects against oleate-induced INS-1E beta cell dysfunction by preserving carbohydrate metabolism. Diabetologia 53 (2): 331-340.
46. Park CW, Kim HW, Ko SH, Usardi A, Bosco D, et al. (2006) Accelerated diabetic nephropathy in mice lacking the peroxisome proliferator-activated receptor alpha. Diabetes 55: 885-893.
47. Hiukka A, Maranghi M, Matikainen N, Taskinen MR, (2010) PPAR alpha: an emerging therapeutic target in diabetic microvascular damage. Nat Rev Endocrinol 6: 454-463.
48. Eskandari HG, Cimen MY, Tamer L, Kanik A, Atik U, (2004) Short term effects of L-carnitine on serum lipids in STZ-induced diabetic rats. Diabetes Res Clin Pract 66: 129-132.
49. Power RA, Hulver MW, Zhang JY, Dubois J, Marchand RM, et al. (2007) Carnitine revisited: potential use as adjunctive treatment in diabetes. Diabetologia 50: 824-832.
50. Ergun O, Ulman C, Kilicalp AS, Ulman I, (2001) Carnitine as a preventive agent in experimental renal ischemia-reperfusion injury. Urol Res 29: 186-189.
51. Farfari S, Schulz V, Corkey B, Prentki M, (2000) Glucose-regulated anaplerosis and cataplerosis in pancreatic beta-cells: possible implication of a pyruvate/citrate shuttle in insulin secretion. Diabetes 49: 718-726.
52. Sun L, Halaihel N, Zhang W, Rogers T, Levi M, (2002) Role of sterol regulatory element-binding protein 1 in regulation of renal lipid metabolism and glomerulosclerosis in diabetes mellitus. J Biol Chem 277: 18919-18927.
53. Kobori M, Masumoto S, Akimoto Y, Oike H, (2011) Chronic dietary intake of quercetin alleviates hepatic fat accumulation associated with consumption of a Western-style diet in C57/BL6J mice. Mol Nutr Food Res 55: 530-540.
54. Navarro-González JF, Mora-Fernández C, de Fuentes MM, García-Pérez J, (2011) Inflammatory molecules and pathways in the pathogenesis of diabetic nephropathy. Nature Reviews Nephrology 7: 327-340.
55. Poulain-Godefroy O, Lecoeur C, Pattou F, Frühbeck G, Froguel P, (2008) Inflammation is associated with a decrease of lipogenic factors in omental fat in women. Am J Physiol Regul Integr Comp Physiol 295: R1-7.
56. Stienstra R, van Diepen JA, Tack CJ, Zaki MH, van de Veerdonk FL, et al. (2011) Inflammasome is a central player in the induction of obesity and insulin resistance. Proc Natl Acad Sci USA 108: 15324-15329.
57. Olusi SO, Al-Awadhi A, Abraham M, (2003) Relations of serum interleukin 18 levels to serum lipid and glucose concentrations in an apparently healthy adult population. Horm Res 60: 29-33.
58. Fink SL, Bergsbaken T, Cookson BT, (2008) Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci USA 105: 4312-4317.
59. Arlehamn CSL, Petrilli V, Gross O, Tschopp J, Evans TJ, (2010) The role of potassium in inflammasome activation by bacteria. J Biol Chem 285: 10508-10518.
60. Poeck H, Bscheider M, Gross O, Finger K, Roth S, et al. (2010) Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat Immunol 11: 63-69.
61. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES, (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458: 509-513.
62. Wu CH, Wu CF, Huang HW, Jao YC, Yen GC, (2009) Naturally occurring flavonoids attenuate high glucose-induced expression of proinflammatory cytokines in human monocytic THP-1 cells. Mol Nutr Food Res 53: 984-995.
63. Kraynak AR, Storer RD, Jensen RD, Kloss MW, Soper KA, et al. (1995) Extent and persistence of streptozotocin-induced DNA damage and cell proliferation in rat kidney as determined by in vivo alkaline elution and BrdUrd labeling assays. Toxicol Appl Pharmacol 135: 279-286.
64. Tesch GH, Allen TJ, (2007) Rodent models of streptozotocin-induced diabetic nephropathy. Nephrology 12: 261-266.
65. Zager RA, Johnson A, Anderson K, Wright S, (2001) Cholesterol ester accumulation: an immediate consequence of acute in vivo ischemic renal injury. Kidney Int 59: 1750-1761.
66. Zager RA, Johnson AC, Hanson SY, (2005) Renal tubular triglyercide accumulation following endotoxic, toxic, and ischemic injury. Kidney Int 67: 111-121.