Beneficial effect of quercetin on cholestatic liver injury

Journal of Nutritional Biochemistry

Volumn 25, Issue 11, 2014, Pages 1183-1195

  Lin, Shih Yi ^a,b   Wang, Ya Yu ^a,b   Chen, Wen Ying ^c   Chuang, Yu Han ^a   Pan, Pin Ho ^d   Chen, Chun Jung ^a,c,e,f  

^a TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^d TUNGS' TAICHUNG METROHARBOR HOSPITAL   (Taiwan)

^e TUNGHAI UNIVERSITY   (Taiwan)

^f HUNGKUANG UNIVERSITY   (Taiwan)

Author keywords

Cholestasis; Fibrosis; Inflammation; Oxidative stress; Quercetin

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; INTERLEUKIN 1BETA; QUERCETIN; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; SMAD2 PROTEIN; SMAD3 PROTEIN; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BILE DUCT LIGATION; CHOLESTASIS; CONTROL GROUP; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; DRUG EFFECT; HEPATITIS; LEUKOCYTE; LIVER FIBROSIS; LIVER HISTOLOGY; LIVER INJURY; LIVER PROTECTION; MALE; MYOFIBROBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; RAT; SERUM; SIGNAL TRANSDUCTION; TREATMENT DURATION; ANIMAL; COMPLICATION; LIVER DISEASES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

ANIMALS; BASE SEQUENCE; CHOLESTASIS; DNA PRIMERS; LIVER DISEASES; MALE; QUERCETIN; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84908250494     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.06.003     Document Type: Article

References (61)

1. Bataller R., Brenner D.A. Liver fibrosis. J Clin Invest 2005, 115:209-218.
2. Desmet V., Roskams T., Van Eyken P. Ductular reaction in the liver. Pathol Res Pract 1995, 191:513-524.
3. Fox E.S., Kim J.C., Tracy T.F. NF-kappaB activation and modulation in hepatic macrophages during cholestatic injury. J Surg Res 1997, 72:129-134.
4. Gäbele E., Froh M., Arteel G.E., Uesugi T., Hellerbrand C., Schölmerich J., et al. TNFα is required for cholestasis-induced liver fibrosis in the mouse. Biochem Biophys Res Commun 2009, 378:348-353.
5. Greim H., Trulzsch D., Roboz J., Dressler K., Czygan P., Hutterer F., et al. Mechanism of cholestasis. Bile acids in normal rat livers and in those after bile duct ligation. Gastroenterology 1972, 63:837-845.
6. Lamireau T., Zoltowska M., Levy E., Yousef I., Rosenbaum J., Tuchweber B., et al. Effects of bile acids on biliary epithelial cells: proliferation, cytotoxicity, and cytokine secretion. Life Sci 2003, 72:1401-1411.
7. Liu T.Z., Lee K.T., Chern C.L., Cheng J.T., Stern A., Tsai L.Y. Free radical-triggered hepatic injury of experimental obstructive jaundice of rats involves overproduction of proinflammatory cytokines and enhanced activation of nuclear factor kappaB. Ann Clin Lab Sci 2001, 31:383-390.
8. Kao T.K., Ou Y.C., Lin S.Y., Pan H.C., Song P.J., Raung S.L., et al. Luteolin inhibits cytokine expression in endotoxin/cytokine-stimulated microglia. J Nutr Biochem 2011, 22:612-624.
9. Kao T.K., Ou Y.C., Raung S.L., Lai C.Y., Liao S.L., Chen C.J. Inhibition of nitric oxide production by quercetin in endotoxin/cytokine-stimulated microglia. Life Sci 2010, 86:315-321.
10. Acquaviva R., Lanteri R., Destri G.L., Caltabiano R., Vanella L., Lanzafame S., et al. Beneficial effects of rutin and l-arginine coadministration in a rat model of liver ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 2009, 296:G664-G670.
11. Dulundu E., Ozel Y., Topaloglu U., Toklu H., Ercan F., Gedik N., et al. Grape seed extract reduces oxidative stress and fibrosis in experimental biliary obstruction. J Gastroenterol Hepatol 2007, 22:885-892.
12. Khan R.A., Khan M.R., Sahreen S. CCl4-induced hepatotoxicity: protective effect of rutin on p53, CYP2E1 and the antioxidative status in rat. BMC Complement Altern Med 2012, 12:478.
13. Tokac M, Taner G, Aydin S, Özkardes AB, Dündar HZ, Taslipinar MY, et al. Protective effects of curcumin against oxidative stress parameters and DNA damage in the livers and kidneys of rats with biliary obstruction. Food Chem Toxicol 2013, 61:28-35.
14. Bharrhan S., Chopra K., Arora S.K., Toor J.S., Rishi P. Down-regulation of NF-κB signaling by polyphenolic compounds prevents endotoxin-induced liver injury in a rat model. Innate Immun 2011, 18:70-79.
15. Choi K.C., Chung W.T., Kwon J.K., Yu J.Y., Jang Y.S., Park S.M., et al. Inhibitory effects of quercetin on aflatoxin B1-induced hepatic damage in mice. Food Chem Toxicol 2010, 48:2747-2753.
16. de David C., Rodrigues G., Bona S., Meurer L., González-Gallego J., Tuñón M.J., et al. Role of quercetin in preventing thioacetamide-induced liver injury in rats. Toxicol Pathol 2011, 39:949-957.
17. Domitronić R., Jakovac H., Vasiliev Marchesi V., Vladimir-Knežević S., Cvijanović O., Tadić Ž., et al. Differential hepatoprotective mechanisms of rutin and quercetin in CCl4-intoxicated BALB/cN mice. Acta Pharmacol Sin 2012, 33:1260-1270.
18. Hernández-Ortega L.D., Alcántar-Díaz B.E., Ruiz-Corro L.A., Sandoval-Rodriguez A., Bueno-Topete M., Armendariz-Borunda J., et al. Quercetin improves hepatic fibrosis reducing hepatic stellate cells and regulating pro-fibrogenic/anti-fibrogenic molecules balance. J Gastroenterol Hepatol 2012, 27:1865-1872.
19. Lee C.C., Shen S.R., Lai Y.J., Wu S.C. Rutin and quercetin, bioactive components from tartary buckwheat, prevent liver inflammatory injury. Food Funct 2013, 4:794-802.
20. Yousef M.I., Omar S.A.M., Ei-Guendi M.I., Abdelmegid L.A. Potential protective effects of quercetin and curcumin on paracetamol-induced histological changes, oxidative stress, impaired liver and kidney functions and haematotoxicity in rat. Food Chem Toxicol 2010, 48:3246-3261.
21. Cuevas M.J., Tieppo J., Marroni N.P., Tuñón M.J., González-Gallego J. Suppression of amphiregulin/epidermal growth factor receptor signals contributes to the protective effects of quercetin in cirrhotic rats. J Nutr 2011, 141:1299-1305.
22. Kanter M. Protective effect of quercetin on liver damage induced by biliary obstruction in rats. J Mol Histol 2010, 41:395-402.
23. Peres W., Tuñón M.J., Collado P.S., Herrmann S., Marroni N.P., González-Gallego J. The flavonoid quercetin ameliorates liver damage in rats with biliary obstruction. J Hepatol 2000, 33:742-750.
24. Vieira E.K., Bona S., Di Naso F.C., Porawski M., Tieppo J., Marroni N.P. Quercetin treatment ameliorates systemic oxidative stress in cirrhotic rats. ISRN Gastroenterol 2011, 2011:604071.
25. Chen W.Y., Lin S.Y., Pan H.C., Liao S.L., Chuang Y.H., Yen Y.J., et al. Beneficial effect of docosahexaenoic acid on cholestatic liver injury in rats. J Nutr Biochem 2012, 23:252-264.
26. Pan P.H., Lin S.Y., Ou Y.C., Chen W.Y., Chuang Y.H., Yen Y.J., et al. Stearic acid attenuates cholestasis-induced liver injury. Biochem Biophys Res Commun 2010, 391:1537-1542.
27. Pan H.C., Kao T.K., Ou Y.C., Yang D.Y., Yen Y.J., Wang C.C., et al. Protective effect of docosahexaenoic acid against brain injury in ischemic rats. J Nutr Biochem 2009, 28:715-725.
28. Rutenberg A.M., Kim H., Fischbein J.W., Hanker J.S., Wasserkrug H.L., Seligman A.M. Histochemical and ultrastructural demonstration of γ-glutamyl transpeptidase activity. J Histochem Cytochem 1969, 17:517-526.
29. Nagase H., Woessner J.F. Matrix metalloproteinases. J Biol Chem 1999, 274:21491-21494.
30. Beaussier M., Wendum D., Schiffer E., Dumont S., Rev C., Lienhart A., et al. Prominent contribution of portal mesenchymal cells to liver fibrosis in ischemic and obstructive cholestatic injuries. Lab Invest 2007, 87:292-303.
31. Bauer M., Schuppan D. TGF-β1 in liver fibrosis: time to change paradigms. FEBS Lett 2001, 502:1-3.
32. Gressner A.M., Weiskirchen R., Breitkopf K., Dooley S. Roles of TGF-beta in hepatic fibrosis. Front Biosci 2002, 7:d793-d807.
33. Kobayashi T., Inoue T., Okada H., Kikuta T., Tanno Y., Nishida T., et al. Connective tissue growth factor mediates the profibrotic effects of transforming growth factor-beta produced by tubular epithelial cells in response to high glucose. Clin Exp Nephrol 2005, 9:114-121.
34. Reyes-Gordillo K., Segovia J., Shibayama M., Tsutsumi V., Vergara P., Moreno M.G., et al. Curcumin prevents and reverses cirrhosis induced by bile duct obstruction or CCl4 in rat: role of TGF-β modulation and oxidative stress. Fundam Clin Pharmacol 2008, 22:417-427.
35. Akira S., Takeda K. Toll-like receptor signaling. Nat Rev Immunol 2004, 4:499-511.
36. Chen A., Zheng S. Curcumin inhibits connective tissue growth factor gene expression in activated hepatic stellate cells in vitro by blocking NF-κB and ERK signaling. Br J Pharmacol 2008, 153:557-567.
37. Poli G., Parola M. Oxidative damage and fibrogenesis. Free Radic Biol Med 1997, 22:287-305.
38. Le Jossic-Corcos C., Duclos S., Ramirez L.C., Zaghini I., Chevillard G., Martin P., et al. Effects of peroxisome proliferator-activated receptor alpha activation on pathways contributing to cholesterol homeostasis in rat hepatocytes. Biochim Biophys Acta 2004, 1683:49-58.
39. Han Y., Haraguchi T., Iwanaga S., Tomotake H., Okazaki Y., Mineo S., et al. Consumption of some polyphenols reduces fecal deoxycholic acid and lithocholic acid, the secondary bile acids of risk factors of colon cancer. J Agric Food Chem 2009, 57:8587-8590.
40. Olaso E., Friedmann S.L. Molecular regulation of hepatic fibrogenesis. J Hepatol 1998, 29:836-847.
41. Williams E.J., Gaca M.D., Brigstock D.R., Arthur M.J., Benyon R.C. Increased expression of connective tissue growth factor in fibrotic human liver and in activated hepatic stellate cells. J Hepatol 2000, 32:754-761.
42. Uchio K., Graham M., Dean N.M., Rosenbaum J., Desmouliere A. Down-regulation of connective tissue growth factor and type I collagen mRNA expression by connective tissue growth factor antisense oligonucleotide during experimental liver fibrosis. Wound Repair Regen 2000, 12:60-66.
43. Demirbilek S., Akm M., Gurunluoglu K., Aydm N.E., Emre M.H., Tas E., et al. The NF-κB inhibitors attenuate hepatic injury in bile duct ligated rats. Pediatr Surg Int 2006, 22:655-663.
44. Baroni G.S., D'Ambrosio L., Ferretti G., Casini A., Sario A.D., Salzano R., et al. Fibrogenic effect of oxidative stress on rat hepatic stellate cells. Hepatology 1998, 27:720-726.
45. Kang C.H., Choi Y.H., Moon S.K., Kim W.J., Kim G.Y. Quercetin inhibits lipopolysaccharide-induced nitric oxide production in BV2 microglial cells by suppressing the NF-κB pathway and activating the Nrf2-dependent HO-1 pathway. Int Immunopharmacol 2013, 17:808-813.
46. Wei-guo Z., Hui Y., Shan L., Yun Z., Wen-cheng N., Fu-lin Y., et al. PPAR-gamma agonist inhibits Ang II-induced activation of dendritic cells via the MAPK and NF-kappaB pathways. Immunol Cell Biol 2010, 88:305-312.
47. Marra F., DeFranco R., Robino G., Novo E., Efsen E., Pastacaldi S., et al. Thiazolidinedione treatment inhibits bile duct proliferation and fibrosis in a rat model of chronic cholestasis. World J Gastroenterol 2005, 11:4931-4938.
48. Kim Y.W., Lee S.M., Shin S.M., Hwang S.J., Brooks J.S., Kang H.E., et al. Efficacy of sauchinone as a novel AMPK-activating lignan for preventing iron-induced oxidative stress and liver injury. Free Radic Biol Med 2009, 47:1082-1092.
49. Shen Y., Croft K.D., Hodgson J.M., Kyle R., Lee I.L., Wang Y., et al. Quercetin and its metabolites improve vessel function by inducing eNOS activity via phosphorylation of AMPK. Biochem Pharmacol 2012, 84:1036-1044.
50. Yan L., Zhang J.D., Wang B., Lv Y.J., Jiang H., Liu G.L., et al. Quercetin inhibits left ventricular hypertrophy in spontaneously hypertensive rats and inhibits angiotensin II-induced H9C2 cells hypertrophy by enhancing PPAR-γ expression and suppressing AP-1 activity. PLoS One 2013, 8:e72548.
51. Seki E., De Minicis S., Osterreicher C.H., Kluwe J., Osawa Y., Brenner D.A., et al. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 2007, 13:1324-1332.
52. Endale M., Park S.C., Kim S., Kim S.H., Yang Y., Cho J.Y., et al. Quercetin disrupts tyrosine-phosphorylated phosphatidylinositol 3-kinase and myeloid differentiation factor-88 association, and inhibits MAPK/AP-1 and IKK/NF-κB-induced inflammatory mediators production in RAW 264.7 cells. Immunobiology 2013, 218:1452-1467.
53. Parkar S.G., Stevenson D.E., Skinner M.A. The potential influence of fruit polyphenols on colonic microflora and human gut health. Int J Food Microbiol 2008, 124:295-298.
54. Wakabayashi Y., Shimizu H., Kimura F., Yoshidome H., Ohtsuka M., Kato A., et al. Mechanism of neutrophil accumulation in sinusoids after extrahepatic biliary obstruction. Hepatogastroenterology 2008, 55:1179-1183.
55. Macmillan-Crow L.A., Cruthirds D.L. Manganese superoxidase dismutase in disease. Free Radic Res 2001, 34:325-336.
56. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2007, 22:659-661.
57. Panchal S.K., Poudyal H., Arumugam T.V., Brown L. Rutin attenuates metabolic changes, nonalcoholic steatohepatitis, and cardiovascular remodeling in high-carbohydrate, high-fat diet-fed rats. J Nutr 2011, 141:1062-1069.
58. Scalbert A., Williamson G. Dietary intake and bioavailability of polyphenols. J Nutr 2000, 130:S2073-S2085.
59. Nakamura Y., Ishimitsu S., Tonogai Y. Effects of quercetin and rutin on serum and hepatic lipid concentrations, fecal steroid excretion and serum antioxidant properties. J Health Sci 2000, 46:229-240.
60. da Silva E.L., Piskula M.K., Yamamoto N., Moon J.H., Terao J. Quercetin metabolites inhibit copper ion-induced lipid peroxidation in rat plasma. FEBS Lett 1998, 430:405-408.
61. Shackelford C., Long G., Wolf J., Okerberg C., Herbert R. Qualitative and quantitative analysis of non-neoplastic lesions in toxicology studies. Toxicol Pathol 2002, 30:93-96.