Quercetin Protects Mice from ConA-Induced Hepatitis by Inhibiting HMGB1-TLR Expression and Down-Regulating the Nuclear Factor Kappa B Pathway

Inflammation

Volumn 39, Issue 1, 2016, Pages 96-106

  Li, Xi ^a   Liu, Hong chun ^a,b   Yao, Qun yan ^a,b   Xu, Bei li ^a,b   Zhang, Shun cai ^a,b   Tu, Chuan tao ^a,b  

^a FUDAN UNIVERSITY   (China)

^b Shanghai Institute of Cardiovascular Diseases   (China)

Author keywords

hepatitis; high mobility group box 1 protein; inflammation; nuclear factor B; quercetin; toll like receptor

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CONCANAVALIN A; GAMMA INTERFERON; HIGH MOBILITY GROUP B1 PROTEIN; I KAPPA B ALPHA; INTERLEUKIN 4; MESSENGER RNA; QUERCETIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; AMINOTRANSFERASE; HMGB1 PROTEIN, MOUSE; I KAPPA B KINASE ALPHA; RELA PROTEIN, MOUSE; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL NUCLEUS; CONCANAVALIN A-INDUCED HEPATITIS; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LIVER NECROSIS; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SINGLE DRUG DOSE; WESTERN BLOTTING; ACTIVE TRANSPORT; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BLOOD; DRUG EFFECTS; GENETICS; HEPATITIS; LIVER; METABOLISM; PATHOLOGY; RANDOMIZATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CONCANAVALIN A; DOWN-REGULATION; HEPATITIS; HMGB1 PROTEIN; INTERFERON-GAMMA; INTERLEUKIN-4; LIVER; MALE; MICE; MICE, INBRED BALB C; NF-KAPPAB INHIBITOR ALPHA; QUERCETIN; RANDOM ALLOCATION; RNA, MESSENGER; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TRANSAMINASES; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84958060386     PISSN: 03603997     EISSN: 15732576     Source Type: Journal    
DOI: 10.1007/s10753-015-0227-9     Document Type: Article

References (44)

1. Thimme, R., S. Wieland, C. Steiger, J. Ghrayeb, K.A. Reimann, R.H. Purcell, et al. 2003. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. Journal of Virology 77: 68–76.
2. Rehermann, B., and M. Nascimbeni. 2005. Immunology of hepatitis B virus and hepatitis C virus infection. Nature Reviews Immunology 5: 215–229.
3. Heneghan, M.A., A.D. Yeoman, S. Verma, A.D. Smith, and M.S. Longhi. 2013. Autoimmune hepatitis. Lancet 382: 1433–1444.
4. Tiegs, G., J. Hentschel, and A. Wendel. 1992. A T cell-dependent experimental liver injury in mice inducible by concanavalin A. Journal of Clinical Investigation 90: 196–203.
5. Ajuebor, M.N., J.A. Carey, and M.G. Swain. 2006. CCR5 in T cell-mediated liver diseases: what’s going on. Journal of Immunology 177: 2039–2045.
6. Kawasuji, A., M. Hasegawa, M. Horikawa, T. Fujita, Y. Matsushita, T. Matsushita, et al. 2006. L-selectin and intercellular adhesion molecule-1 regulate the development of concanavalin A-induced liver injury. Journal of Leukocyte Biology 79: 696–705.
7. Wang, H., O. Bloom, M. Zhang, J.M. Vishnubhakat, M. Ombrellino, J. Che, et al. 1999. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285: 248–251.
8. Lotze, M.T., and K.J. Tracey. 2005. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nature Reviews Immunology 5: 331–342.
9. Andersson, U., and K.J. Tracey. 2011. HMGB1 is a therapeutic target for sterile inflammation and infection. Annual Review of Immunology 29: 139–162.
10. Musumeci, D., G.N. Roviello, and D. Montesarchio. 2014. An overview on HMGB1 inhibitors as potential therapeutic agents in HMGB1-related pathologies. Pharmacology and Therapeutics 141: 347–357.
11. Baldwin Jr., A.S. 1996. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annual Review of Immunology 14: 649–683.
12. Sass, G., S. Heinlein, A. Agli, R. Bang, J. Schumann, and G. Tiegs. 2002. Cytokine expression in three mouse models of experimental hepatitis. Cytokine 19: 115–120.
13. Tsung, A., J.R. Klune, X. Zhang, G. Jeyabalan, Z. Cao, X. Peng, et al. 2007. HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. Journal of Experimental Medicine 204: 2913–2923.
14. Gong, Q., H. Zhang, J.H. Li, L.H. Duan, S. Zhong, X.L. Kong, et al. 2010. High-mobility group box 1 exacerbates concanavalin A-induced hepatic injury in mice. International Journal of Molecular Medicine (Berl) 88: 1289–1298.
15. Takano, K., M. Shinoda, M. Tanabe, T. Miyasho, S. Yamada, S. Ono, et al. 2010. Protective effect of high-mobility group box 1 blockade on acute liver failure in rats. Shock 34: 573–579.
16. Zhou, R.R., S.S. Zhao, M.X. Zou, P. Zhang, B.X. Zhang, X.H. Dai, et al. 2011. HMGB1 cytoplasmic translocation in patients with acute liver failure. BMC Gastroenterology 11: 21.
17. Tu, C.T., Q.Y. Yao, B.L. Xu, and S.C. Zhang. 2013. Curcumin protects against concanavalin A-induced hepatitis in mice through inhibiting the cytoplasmic translocation and expression of high mobility group box 1. Inflammation 36: 206–215.
18. Schwabe, R.F., E. Seki, and D.A. Brenner. 2006. Toll-like receptor signaling in the liver. Gastroenterology 130: 1886–1900.
19. Ojiro, K., H. Ebinuma, N. Nakamoto, K. Wakabayashi, Y. Mikami, Y. Ono, et al. 2010. MyD88-dependent pathway accelerates the liver damage of Concanavalin A-induced hepatitis. Biochemical and Biophysical Research Communications 399: 744–749.
20. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805–820.
21. Xu, J., X. Zhang, M. Monestier, N.L. Esmon, and C.T. Esmon. 2011. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. Journal of Immunology 187: 2626–2631.
22. Tu, C.T., B. Han, Q.Y. Yao, Y.A. Zhang, H.C. Liu, and S.C. Zhang. 2012. Curcumin attenuates Concanavalin A-induced liver injury in mice by inhibition of toll-like receptor (TLR) 2, TLR4 and TLR9 expression. International Immunopharmacology 12: 151–157.
23. Formica, J.V., and W. Regelson. 1995. Review of the biology of quercetin and related bioflavonoids. Food and Chemical Toxicology 33: 1061–1080.
24. Del, P.A., A. Scalera, M.D. Iadevaia, A. Miranda, C. Zulli, L. Gaeta, et al. 2012. Herbal products: benefits, limits, and applications in chronic liver disease. Evidence-based Complementary and Alternative Medicine 2012: 837939.
25. Bhaskar, S., V. Shalini, and A. Helen. 2011. Quercetin regulates oxidized LDL induced inflammatory changes in human PBMCs by modulating the TLR-NF-kappaB signaling pathway. Immunobiology 216: 367–373.
26. Marcolin, E., B. San-Miguel, D. Vallejo, J. Tieppo, N. Marroni, J. Gonzalez-Gallego, et al. 2012. Quercetin treatment ameliorates inflammation and fibrosis in mice with nonalcoholic steatohepatitis. Journal of Nutrition 142: 1821–1828.
27. Byun, E.B., M.S. Yang, H.G. Choi, N.Y. Sung, D.S. Song, S.J. Sin, et al. 2013. Quercetin negatively regulates TLR4 signaling induced by lipopolysaccharide through Tollip expression. Biochemical and Biophysical Research Communications 431: 698–705.
28. Tang, D., R. Kang, W. Xiao, H. Zhang, M.T. Lotze, H. Wang, et al. 2009. Quercetin prevents LPS-induced high-mobility group box 1 release and proinflammatory function. American Journal of Respiratory Cell and Molecular Biology 41: 651–660.
29. Su, J.F., C.J. Guo, J.Y. Wei, J.J. Yang, Y.G. Jiang, and Y.F. Li. 2003. Protection against hepatic ischemia-reperfusion injury in rats by oral pretreatment with quercetin. Biomedical and Environmental Sciences 16: 1–8.
30. de David, C., G. Rodrigues, S. Bona, L. Meurer, J. Gonzalez-Gallego, M.J. Tunon, et al. 2011. Role of quercetin in preventing thioacetamide-induced liver injury in rats. Toxicologic Pathology 39: 949–957.
31. Domitrovic, R., H. Jakovac, M.V. Vasiljev, S. Vladimir-Knezevic, O. Cvijanovic, Z. Tadic, et al. 2012. Differential hepatoprotective mechanisms of rutin and quercetin in CCl (4)-intoxicated BALB/cN mice. Acta Pharmacologica Sinica 33: 1260–1270.
32. Yumoto, E., T. Higashi, K. Nouso, H. Nakatsukasa, K. Fujiwara, T. Hanafusa, et al. 2002. Serum gamma-interferon-inducing factor (IL-18) and IL-10 levels in patients with acute hepatitis and fulminant hepatic failure. Journal of Gastroenterology and Hepatology 17: 285–294.
33. Castellano-Higuera, A., E. Gonzalez-Reimers, M.R. Aleman-Valls, P. Abreu-Gonzalez, F. Santolaria-Fernandez, M.J. De La Vega-Prieto, et al. 2008. Cytokines and lipid peroxidation in alcoholics with chronic hepatitis C virus infection. Alcohol and Alcoholism 43: 137–142.
34. Zou, Z., B. Li, D. Xu, Z. Zhang, J.M. Zhao, G. Zhou, et al. 2009. Imbalanced intrahepatic cytokine expression of interferon-gamma, tumor necrosis factor-alpha, and interleukin-10 in patients with acute-on-chronic liver failure associated with hepatitis B virus infection. Journal of Clinical Gastroenterology 43: 182–190.
35. Park, J.S., D. Svetkauskaite, Q. He, J.Y. Kim, D. Strassheim, A. Ishizaka, et al. 2004. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. Journal of Biological Chemistry 279: 7370–7377.
36. Chen, Y., and R. Sun. 2011. Toll-like receptors in acute liver injury and regeneration. International Immunopharmacology 11: 1433–1441.
37. Uesugi, T., M. Froh, G.E. Arteel, B.U. Bradford, and R.G. Thurman. 2001. Toll-like receptor 4 is involved in the mechanism of early alcohol-induced liver injury in mice. Hepatology 34: 101–108.
38. Xiao, X., P. Zhao, D. Rodriguez-Pinto, D. Qi, O. Henegariu, L. Alexopoulou, et al. 2009. Inflammatory regulation by TLR3 in acute hepatitis. Journal of Immunology 183: 3712–3719.
39. Luedde, T., and R.F. Schwabe. 2011. NF-kappaB in the liver—linking injury, fibrosis and hepatocellular carcinoma. Nature Reviews Gastroenterology & Hepatology 8: 108–118.
40. Schumann, J., J. Prockl, A.K. Kiemer, A.M. Vollmar, R. Bang, and G. Tiegs. 2003. Silibinin protects mice from T cell-dependent liver injury. Journal of Hepatology 39: 333–340.
41. Hoffmann, F., G. Sass, J. Zillies, S. Zahler, G. Tiegs, A. Hartkorn, et al. 2009. A novel technique for selective NF-kappaB inhibition in Kupffer cells: contrary effects in fulminant hepatitis and ischaemia-reperfusion. Gut 58: 1670–1678.
42. Comalada, M., D. Camuesco, S. Sierra, I. Ballester, J. Xaus, J. Galvez, et al. 2005. In vivo quercitrin anti-inflammatory effect involves release of quercetin, which inhibits inflammation through down-regulation of the NF-kappaB pathway. European Journal of Immunology 35: 584–592.
43. Bharrhan, S., K. Chopra, S.K. Arora, J.S. Toor, and P. Rishi. 2012. Down-regulation of NF-kappaB signalling by polyphenolic compounds prevents endotoxin-induced liver injury in a rat model. Innate Immunity 18: 70–79.
44. Liu, H., C.R. Lo, and M.J. Czaja. 2002. NF-kappaB inhibition sensitizes hepatocytes to TNF-induced apoptosis through a sustained activation of JNK and c-Jun. Hepatology 35: 772–778.