Role of Nrf2 activation and NF-κB inhibition in valproic acid induced hepatotoxicity and in diammonium glycyrrhizinate induced protection in mice

Food and Chemical Toxicology

Volumn 73, Issue , 2014, Pages 95-104

  Jin, Jing ^a   Xiong, Tianqin ^b   Hou, Xiangyu ^a   Sun, Xiaozhe ^a   Liao, Jiayi ^b   Huang, Zhiying ^a   Huang, Min ^a   Zhao, Zhongxiang ^b  

^a SUN YAT SEN UNIVERSITY   (China)

^b GUANGZHOU UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Cytokines; Diammonium glycyrrhizinate; Hepatotoxicity; NF B; Nrf2; Valproic acid

Indexed keywords

CYTOKINE; DIAMMONIUM GLYCYRRHIZINATE; GLUTATHIONE; GLYCYRRHIZIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; VALPROIC ACID; ANTICONVULSIVE AGENT; AUTACOID; NFE2L2 PROTEIN, MOUSE; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; LIVER DYSFUNCTION; LIVER INJURY; LIVER PROTECTION; LIVER TOXICITY; MALE; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION REGULATION; HEPG2 CELL LINE; LIVER; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

MUS;

ANIMALS; ANTICONVULSANTS; BASE SEQUENCE; CYTOKINES; DNA PRIMERS; GENE EXPRESSION REGULATION; GLYCYRRHIZIC ACID; HEP G2 CELLS; HUMANS; INFLAMMATION MEDIATORS; LIVER; MICE; MICE, INBRED BALB C; NF-E2-RELATED FACTOR 2; NF-KAPPA B; REAL-TIME POLYMERASE CHAIN REACTION; VALPROIC ACID;

EID: 84908071557     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2014.08.009     Document Type: Article

References (43)

1. Aires C.C.P., van Cruchten A., Ijlst L., de Almeida I.T., Duran M., Wanders R.J.A., Silva M.F.B. New insights on the mechanisms of valproate-induced hyperammonemia: inhibition of hepatic N-acetylglutamate synthase activity by valproyl-CoA. J. Hepatol. 2011, 55:426-434.
2. Akao T., Hayashi T., Kobashi K., Kanaoka M., Kato H., Kobayashi M., Takeda S., Oyama T. Intestinal bacterial hydrolysis is indispensable to absorption of 18 beta-glycyrrhetic acid after oral administration of glycyrrhizin in rats. J. Pharm. Pharmacol. 1994, 46:135-137.
3. Baird L., Dinkova-Kostova A.T. The cytoprotective role of the Keap1-Nrf2 pathway. Arch. Toxicol. 2011, 85:241-272.
4. Boesch-Saadatmandi C., Wagner A.E., Graeser A.C., Hundhausen C., Wolffram S., Rimbach G. Ochratoxin A impairs Nrf2-dependent gene expression in porcine kidney tubulus cells. J. Anim. Physiol. Anim. Nutr. 2009, 93:547-554.
5. Chang T.K., Abbott F.S. Oxidative stress as a mechanism of valproic acid-associated hepatotoxicity. Drug Metab. Rev. 2006, 38:627-639.
6. Cho B.O., Ryu H.W., Jin C.H., Choi D.S., Kang S.Y., Kim D.S., Byun M.W., Jeong I.Y. Blackberry extract attenuates oxidative stress through up-regulation of Nrf2-dependent antioxidant enzymes in carbon tetrachloride-treated rats. J. Agric. Food. Chem. 2011, 59:11442-11448.
7. Chu X.M., Zhang L.F., Wang G.J., Zhang S.N., Zhou J.H., Hao H.P. Influence of UDP-glucuronosyltransferase polymorphisms on valproic acid pharmacokinetics in Chinese epilepsy patients. Eur. J. Clin. Pharmacol. 2012, 68:1395-1401.
8. Das J., Ghosh J., Roy A., Sil P.C. Mangiferin exerts hepatoprotective activity against D-galactosamine induced acute toxicity and oxidative/nitrosative stress via Nrf2-NFkappaB pathways. Toxicol. Appl. Pharmacol. 2012, 260:35-47.
9. Diehl A.M. Cytokine regulation of liver injury and repair. Immunol. Rev. 2000, 174:160-171.
10. Dorn C., Heilmann J., Hellerbrand C. Protective effect of xanthohumol on toxin-induced liver inflammation and fibrosis. Int. J. Clin. Exp. Pathol. 2012, 5:29-36.
11. Enomoto A., Itoh K., Nagayoshi E., Haruta J., Kimura T., O'Connor T., Harada T., Yamamoto M. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol. Sci. 2001, 59:169-177.
12. Feng C., Wang H., Yao C., Zhang J., Tian Z. Diammonium glycyrrhizinate, a component of traditional Chinese medicine Gan-Cao, prevents murine T-cell-mediated fulminant hepatitis in IL-10- and IL-6-dependent manners. Int. Immunopharmacol. 2007, 7:1292-1298.
13. Fisher R., Nau H., Gandolfi A.J., Putnam C.W., Brendel K. Valproic acid hepatotoxicity in human liver slices. Drug Chem. Toxicol. 1991, 14:375-394.
14. Furnari M.A. Behavioral, neurochemical, and neuroimmune changes in NRF2 knockout mice following early postnatal exposure to valproic acid 2013, 1-176. Rutgers The State University of New Jersey - New Brunswick and University of Medicine and Dentistry of New Jersey, Ann Arbor, United States.
15. Garcia-Morales I., Sancho Rieger J., Gil-Nagel A., Herranz Fernandez J.L. Antiepileptic drugs: from scientific evidence to clinical practice. Neurologist 2007, 13:S20-S28.
16. Ghozzi H., Hakim A., Sahnoun Z., Ben Mahmoud L., Atheymen R., Hammami S., Zeghal K. Relationship between plasma concentrations of valproic acid and hepatotoxicity in patients receiving high doses. Rev. Neurol. (Paris) 2011, 167:600-606.
17. Haddad P.M., Das A., Ashfaq M., Wieck A. A review of valproate in psychiatric practice. Expert Opin. Drug Metab. Toxicol. 2009, 5:539-551.
18. Hou S.Z., Li Y., Zhu X.L., Wang Z.Y., Wang X., Xu Y. Ameliorative effects of diammonium glycyrrhizinate on inflammation in focal cerebral ischemic-reperfusion injury. Brain Res. 2012, 1447:20-27.
19. Jin H.H., Zheng G.P., Chen W.R., Liu D., Cheng X., Ren J.B. The use of diammonium glycyrrhizinate in the treatment of hepatic dysfunction in burn patients. Zhonghua Shao Shang Za Zhi 2005, 21:353-355.
20. Jin W., Wang H., Yan W., Xu L., Wang X., Zhao X., Yang X., Chen G., Ji Y. Disruption of Nrf2 enhances upregulation of nuclear factor-kappaB activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury. Mediators Inflamm. 2008, 2008:725174.
21. Kiang T.K., Teng X.W., Karagiozov S., Surendradoss J., Chang T.K., Abbott F.S. Role of oxidative metabolism in the effect of valproic acid on markers of cell viability, necrosis, and oxidative stress in sandwich-cultured rat hepatocytes. Toxicol. Sci. 2010, 118:501-509.
22. Kiang T.K., Teng X.W., Surendradoss J., Karagiozov S., Abbott F.S., Chang T.K. Glutathione depletion by valproic acid in sandwich-cultured rat hepatocytes: role of biotransformation and temporal relationship with onset of toxicity. Toxicol. Appl. Pharmacol. 2011, 252:318-324.
23. Klaassen C.D., Reisman S.A. Nrf2 the rescue: effects of the antioxidative/electrophilic response on the liver. Toxicol. Appl. Pharmacol. 2010, 244:57-65.
24. Kobayashi M., Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signaling 2005, 7:385-394.
25. Lamle J., Marhenke S., Borlak J., von Wasielewski R., Eriksson C.J., Geffers R., Manns M.P., Yamamoto M., Vogel A. Nuclear factor-eythroid 2-related factor 2 prevents alcohol-induced fulminant liver injury. Gastroenterology 2008, 134:1159-1168.
26. Lee I.C., Kim S.H., Baek H.S., Moon C., Kang S.S., Kim Y.B., Shin I.S., Kim J.C. The involvement of Nrf2 in the protective effects of diallyl disulfide on carbon tetrachloride-induced hepatic oxidative damage and inflammatory response in rats. Food Chem. Toxicol. 2014, 63:174-185.
27. Leiro J., Arranz J.A., Yanez M., Ubeira F.M., Sanmartin M.L., Orallo F. Expression profiles of genes involved in the mouse nuclear factor-kappaB signal transduction pathway are modulated by mangiferin. Int. Immunopharmacol. 2004, 4:763-778.
28. Li Q.Z., Li D.J., Zhi L.Q. Systematic review of diammonium glycyrrhizinate in the treatment of drug-induced liver injury. China Pharm. 2010, 21:1100-1105.
29. Liu L.L., Gong L.K., Wang H., Xiao Y., Wu X.F., Zhang Y.H., Xue X., Qi X.M., Ren J. Baicalin protects mouse from Concanavalin A-induced liver injury through inhibition of cytokine production and hepatocyte apoptosis. Liver Int. 2007, 27:582-591.
30. Lu Y., Zhu J., Chen X., Li N., Fu F., He J., Wang G., Zhang L., Zheng Y., Qiu Z., Yu X., Han D., Wu L. Identification of human UDP-glucuronosyltransferase isoforms responsible for the glucuronidation of glycyrrhetinic acid. Drug Metab. Pharmacokinet. 2009, 24:523-528.
31. Nanau R.M., Neuman M.G. Adverse drug reactions induced by valproic acid. Clin. Biochem. 2013, 46:1323-1338.
32. Palsamy P., Bidasee K.R., Shinohara T. Valproic acid suppresses Nrf2/Keap1 dependent antioxidant protection through induction of endoplasmic reticulum stress and Keap1 promoter DNA demethylation in human lens epithelial cells. Exp. Eye Res. 2014, 121:26-34.
33. Ramadori G., Armbrust T. Cytokines in the liver. Eur. J. Gastroenterol. Hepatol. 2001, 13:777-784.
34. Reisman S.A., Buckley D.B., Tanaka Y., Klaassen C.D. CDDO-Im protects from acetaminophen hepatotoxicity through induction of Nrf2-dependent genes. Toxicol. Appl. Pharmacol. 2009, 236:109-114.
35. Reyes-Gordillo K., Segovia J., Shibayama M., Vergara P., Moreno M.G., Muriel P. Curcumin protects against acute liver damage in the rat by inhibiting NF-kappaB, proinflammatory cytokines production and oxidative stress. Biochim. Biophys. Acta 2007, 1770:989-996.
36. Sokmen B.B., Tunali S., Yanardag R. Effects of vitamin U (S-methyl methionine sulphonium chloride) on valproic acid induced liver injury in rats. Food Chem. Toxicol. 2012, 50:3562-3566.
37. Sugimoto T., Woo M., Nishida N., Takeuchi T., Sakane Y., Kobayashi Y. Hepatotoxicity in rat following administration of valproic acid. Epilepsia 1987, 28:142-146.
38. Surh Y.J., Na H.K. NF-kappaB and Nrf2 as prime molecular targets for chemoprevention and cytoprotection with anti-inflammatory and antioxidant phytochemicals. Genes Nutr. 2008, 2:313-317.
39. Thimmulappa R.K., Lee H., Rangasamy T., Reddy S.P., Yamamoto M., Kensler T.W., Biswal S. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J. Clin. Investig. 2006, 116:984-995.
40. Tong V., Teng X.W., Chang T.K., Abbott F.S. Valproic acid I: time course of lipid peroxidation biomarkers, liver toxicity, and valproic acid metabolite levels in rats. Toxicol. Sci. 2005, 86:427-435.
41. Tong V., Teng X.W., Chang T.K., Abbott F.S. Valproic acid II: effects on oxidative stress, mitochondrial membrane potential, and cytotoxicity in glutathione-depleted rat hepatocytes. Toxicol. Sci. 2005, 86:436-443.
42. Wu K.C., Liu J.J., Klaassen C.D. Nrf2 activation prevents cadmium-induced acute liver injury. Toxicol. Appl. Pharmacol. 2012, 263:14-20.
43. Zhu X., Chen C., Ye D., Guan D., Ye L., Jin J., Zhao H., Chen Y., Wang Z., Wang X., Xu Y. Diammonium glycyrrhizinate upregulates PGC-1alpha and protects against Abeta1-42-induced neurotoxicity. PLoS ONE 2012, 7:e35823.