Troxerutin inhibits 2,2',4,4'-tetrabromodiphenyl ether (BDE-47)-induced hepatocyte apoptosis by restoring proteasome function

Toxicology Letters

Volumn 233, Issue 3, 2015, Pages 246-257

  Zhang, Zi Feng ^a,b   Shan, Qun ^a,b   Zhuang, Juan ^a   Zhang, Yan Qiu ^a   Wang, Xin ^b,c   Fan, Shao Hua ^b   Lu, Jun ^b   Wu, Dong Mei ^b   Hu, Bin ^b   Zheng, Yuan Lin ^b  

^a CHINA UNIVERSITY OF MINING AND TECHNOLOGY   (China)

^b JIANGSU NORMAL UNIVERSITY   (China)

^c Jiangsu Xuzhou Sweetpotato Research Centre   (China)

Author keywords

Endoplasmic reticulum stress; Hepatocyte apoptosis; Oxidative stress; Polybrominated diphenyl ethers; Proteasome dysfunction; Troxerutin

Indexed keywords

2,2',4,4' TETRABROMODIPHENYL ETHER; ALANINE AMINOTRANSFERASE; APOPTOSIS SIGNAL REGULATING KINASE 1; CASPASE 3; CHYMOTRYPSIN; EPOXOMICIN; INITIATION FACTOR 2ALPHA; PERK PROTEIN; POLYBROMINATED DIPHENYL ETHER; PROTEASOME; PROTEIN; PROTEIN BCL 2; PROTEIN IRE1; TROXERUTIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG; 2,2',4,4'-TETRABROMODIPHENYL ETHER; DIPHENYL ETHER DERIVATIVE; MONOXERUTIN; OLIGOPEPTIDE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; LIVER; LIVER CELL; LIVER INJURY; LIVER PROTECTION; LIVER TOXICITY; MALE; MOUSE; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; INSTITUTE FOR CANCER RESEARCH MOUSE; PATHOLOGY; PHYSIOLOGY;

MUS;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; HALOGENATED DIPHENYL ETHERS; HEPATOCYTES; HYDROXYETHYLRUTOSIDE; MALE; MICE; MICE, INBRED ICR; OLIGOPEPTIDES; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 84922370578     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.01.017     Document Type: Article

References (49)

1. Aiken C.T., Kaake R.M., Wang X., Huang L. Oxidative stress-mediated regulation of proteasome complexes. Mol. Cell. Proteomics 2011, 10. R110.006924.
2. Arshad M., Ye Z., Gu X., Wong C.K., Liu Y., Li D., Zhou L., Zhang Y., Bay W.P., Yu V.C., Li P. RNF13, a RING finger protein, mediates endoplasmic reticulum stress-induced apoptosis through the inositol-requiring enzyme (IRE1α)/c-Jun NH2-terminal kinase pathway. J. Biol. Chem. 2013, 288:8726-8736.
3. Blasig I.E., Loewe H., Ebert B. Effect of troxerutin and methionine on spin trapping of free oxy-radicals. Biomed. Biochim. Acta 1988, 47:S252-S255.
4. Brodsky M., Hirsh S., Albeck M., Sredni B. Resolution of inflammation-related apoptotic processes by the synthetic tellurium compound, AS101 following liver injury. J. Hepatol. 2009, 51:491-503.
5. Chen H.Y., Ren X.Y., Wang W.H., Zhang Y.X., Chen S.F., Zhang B., Wang L.X. Upregulated ROS production induced by the proteasome inhibitor MG-132 on XBP1 gene expression and cell apoptosis in Tca-8113 cells. Biomed. Pharmacother. 2014, 68:709-713.
6. Chhunchha B., Fatma N., Kubo E., Rai P., Singh S.P., Singh D.P. Curcumin abates hypoxia-induced oxidative stress based-ER stress-mediated cell death in mouse hippocampal cells (HT22) by controlling Prdx6 and NF-κB regulation. Am. J. Physiol. Cell Physiol. 2013, 304:C636-C655.
7. Dunnick J.K., Nyska A. Characterization of liver toxicity in F344/N rats and B6C3F1 mice after exposure to a flame retardant containing lower molecular weight polybrominated diphenyl ethers. Exp. Toxicol. Pathol. 2009, 61:1-12.
8. Fan S.H., Zhang Z.F., Zheng Y.L., Lu J., Wu D.M., Shan Q., Hu B., Wang Y.Y. Troxerutin protects the mouse kidney from d-galactose-caused injury through anti-inflammation and anti-oxidation. Int. Immunopharmacol. 2009, 9:91-96.
9. Farout L., Friguet B. Proteasome function in aging and oxidative stress: implications in protein maintenance failure. Antioxid. Redox Signal. 2006, 8:205-216.
10. He P., Wang A.G., Xia T., Gao P., Niu Q., Guo L.J., Chen X.M. Mechanisms underlying the developmental neurotoxic effect of PBDE-47 and the enhanced toxicity associated with its combination with PCB153 in rats. Neurotoxicology 2009, 30:1088-1095.
11. Herrmann J., Wohlert C., Saguner A.M., Flores A., Nesbitt L.L., Chade A., Lerman L.O., Lerman A. Primary proteasome inhibition results in cardiac dysfunction. Eur. J. Heart Fail. 2013, 15:614-623.
12. Hoffman K., Adgent M., Goldman B.D., Sjödin A., Daniels J.L. Lactational exposure to polybrominated diphenyl ethers and its relation to social and emotional development among toddlers. Environ. Health Perspect. 2012, 120:1438-1442.
13. Jiang C., Zhang S., Liu H., Zeng Q., Xia T., Chen Y., Kuang G., Zhao G., Wu X., Zhang X., Wang A. The role of the IRE1 pathway in PBDE-47-induced toxicity in human neuroblastoma SH-SY5Y cells in vitro. Toxicol. Lett. 2012, 211:325-333.
14. Jin S., Yang F., Hui Y., Xu Y., Lu Y., Liu J. Cytotoxicity and apoptosis induction on RTG-2 cells of 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) and decabrominated diphenyl ether (BDE-209). Toxicol. In Vitro 2010, 24:1190-1196.
15. Kessler M., Ubeaud G., Walter T., Sturm F., Jung L. Free radical scavenging and skin penetration of troxerutin and vitamin derivatives. J. Dermatolog. Treat. 2002, 13:133-141.
16. Kim U.J., Kim M.Y., Hong Y.H., Lee D.H., Oh J.E. Assessment of impact of internal exposure to PBDEs on human thyroid function-comparison between congenital hypothyroidism and normal paired blood. Environ. Sci. Technol. 2012, 46:6261-6268.
17. Kwak M.K., Wakabayashi N., Greenlaw J.L., Yamamoto M., Kensler T.W. Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol. Cell Biol. 2003, 23:8786-8794.
18. Kwak M.K., Cho J.M., Huang B., Shin S., Kensler T.W. Role of increased expression of the proteasome in the protective effects of sulforaphane against hydrogen peroxide-mediated cytotoxicity in murine neuroblastoma cells. Free Radic. Biol. Med. 2007, 43:809-817.
19. Launay N., Ruiz M., Fourcade S., Schlüter A., Guilera C., Ferrer I., Knecht E., Pujol A. Oxidative stress regulates the ubiquitin-proteasome system and immunoproteasome functioning in a mouse model of X-adrenoleukodystrophy. Brain 2013, 136:891-904.
20. Lee C.S., Ho D.V., Chan J.Y. Nuclear factor-erythroid 2-related factor 1 regulates expression of proteasome genes in hepatocytes and protects against endoplasmic reticulum stress and steatosis in mice. FEBS J. 2013, 280:3609-3620.
21. Liu Y., Shen S., Li Z., Jiang Y., Si J., Chang Q., Liu X., Pan R. Cajaninstilbene acid protects corticosterone-induced injury in PC12 cells by inhibiting oxidative and endoplasmic reticulum stress-mediated apoptosis. Neurochem. Int. 2014, 78C:43-52.
22. Lu J., Wu D.M., Zheng Z.H., Zheng Y.L., Hu B., Zhang Z.F. Troxerutin protects against high cholesterol-induced cognitive deficits in mice. Brain 2011, 134:783-797.
23. Lu J., Wu D.M., Zheng Y.L., Hu B., Cheng W., Zhang Z.F., Li M.Q. Troxerutin counteracts domoic acid-induced memory deficits in mice by inhibiting CCAAT/enhancer binding protein β-mediated inflammatory response and oxidative stress. J. Immunol. 2013, 190:3466-3479.
24. Maher P. The flavonoid fisetin promotes nerve cell survival from trophic factor withdrawal by enhancement of proteasome activity. Arch. Biochem. Biophys. 2008, 476:139-144.
25. Malhotra D., Thimmulappa R., Vij N., Navas-Acien A., Sussan T., Merali S., Zhang L., Kelsen S.G., Myers A., Wise R., Tuder R., Biswal S. Heightened endoplasmic reticulum stress in the lungs of patients with chronic obstructive pulmonary disease: the role of Nrf2-regulated proteasomal activity. Am. J. Respir. Crit. Care Med. 2009, 180:1196-1207.
26. Maranghi F., Tassinari R., Moracci G., Altieri I., Rasinger J.D., Carroll T.S., Hogstrand C., Lundebye A.K., Mantovani A. Dietary exposure of juvenile female mice to polyhalogenated seafood contaminants (HBCD BDE-47, PCB-153, TCDD): comparative assessment of effects in potential target tissues. Food Chem. Toxicol. 2013, 56:443-449.
27. Novoa I., Zeng H., Harding H.P., Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell Biol. 2001, 153:1011-1022.
28. Otoda T., Takamura T., Misu H., Ota T., Murata S., Hayashi H., Takayama H., Kikuchi A., Kanamori T., Shima K.R., Lan F., Takeda T., Kurita S., Ishikura K., Kita Y., Iwayama K., Kato K., Uno M., Takeshita Y., Yamamoto M., Tokuyama K., Iseki S., Tanaka K., Kaneko S. Proteasome dysfunction mediates obesity-induced endoplasmic reticulum stress and insulin resistance in the liver. Diabetes 2013, 62:811-824.
29. Puthalakath H., O'Reilly L.A., Gunn P., Lee L., Kelly P.N., Huntington N.D., Hughes P.D., Michalak E.M., McKimm-Breschkin J., Motoyama N., Gotoh T., Akira S., Bouillet P., Strasser A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129:1337-1349.
30. Richardson V.M., Staskal D.F., Ross D.G., Diliberto J.J., DeVito M.J., Birnbaum L.S. Possible mechanisms of thyroid hormone disruption in mice by BDE 47: a major polybrominated diphenyl ether congener. Toxicol. Appl. Pharmacol. 2008, 226:244-250.
31. Shang F., Taylor A. Ubiquitin-proteasome pathway and cellular responses to oxidative stress. Free Radic. Biol. Med. 2011, 51:5-16.
32. Shao J., White C.C., Dabrowski M.J., Kavanagh T.J., Eckert M.L., Gallagher E.P. The role of mitochondrial and oxidative injury in BDE 47 toxicity to human fetal liver hematopoietic stem cells. Toxicol. Sci. 2008, 101:81-90.
33. Shen M., Wang L., Yang G., Gao L., Wang B., Guo X., Zeng C., Xu Y., Shen L., Cheng K., Xia Y., Li X., Wang H., Fan L., Wang X. Baicalin protects the cardiomyocytes from ER stress-induced apoptosis: inhibition of CHOP through induction of endothelial nitric oxide synthase. PLoS One 2014, 9:e88389.
34. Shukla R.K., Kumar A., Gurbani D., Pandey A.K., Singh S., Dhawan A. TiO(2) nanoparticles induce oxidative DNA damage and apoptosis in human liver cells. Nanotoxicology 2013, 7:48-60.
35. Song E., Fu J., Xia X., Su C., Song Y. Bazhen decoction protects against acetaminophen induced acute liver injury by inhibiting oxidative stress, inflammation and apoptosis in mice. PLoS One 2014, 9:e107405.
36. Song R., Duarte T.L., Almeida G.M., Farmer P.B., Cooke M.S., Zhang W., Sheng G., Fu J., Jones G.D. Cytotoxicity and gene expression profiling of two hydroxylated polybrominated diphenyl ethers in human H295R adrenocortical carcinoma cells. Toxicol. Lett. 2009, 185:23-31.
37. Sueyoshi T., Li L., Wang H., Moore R., Kodavanti P.R., Lehmler H.J., Negishi M., Birnbaum L.S. Flame retardant BDE-47 effectively activates nuclear receptor CAR in human primary hepatocytes. Toxicol. Sci. 2014, 137:292-302.
38. Sun F., Anantharam V., Latchoumycandane C., Kanthasamy A., Kanthasamy A.G. Dieldrin induces ubiquitin-proteasome dysfunction in alpha-synuclein overexpressing dopaminergic neuronal cells and enhances susceptibility to apoptotic cell death. J. Pharmacol. Exp. Ther. 2005, 315:69-79.
39. Sun F., Kanthasamy A., Anantharam V., Kanthasamy A.G. Environmental neurotoxic chemicals-induced ubiquitin proteasome system dysfunction in the pathogenesis and progression of Parkinson's disease. Pharmacol. Ther. 2007, 114:327-344.
40. Tagliaferri S., Caglieri A., Goldoni M., Pinelli S., Alinovi R., Poli D., Pellacani C., Giordano G., Mutti A., Costa L.G. Low concentrations of the brominated flame retardants BDE-47 and BDE-99 induce synergistic oxidative stress-mediated neurotoxicity in human neuroblastoma cells. Toxicol. In Vitro 2010, 24:116-122.
41. Uehara T., Nakamura T., Yao D., Shi Z.Q., Gu Z., Ma Y., Masliah E., Nomura Y., Lipton S.A. S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 2006, 441:513-517.
42. Wang K. Molecular mechanisms of hepatic apoptosis. Cell Death Dis. 2014, 5:e996.
43. Wang L., Zou W., Zhong Y., An J., Zhang X., Wu M., Yu Z. The hormesis effect of BDE-47 in HepG2 cells and the potential molecular mechanism. Toxicol. Lett. 2012, 209:193-201.
44. Woods R., Vallero R.O., Golub M.S., Suarez J.K., Ta T.A., Yasui D.H., Chi L.H., Kostyniak P.J., Pessah I.N., Berman R.F., LaSalle J.M. Long-lived epigenetic interactions between perinatal PBDE exposure and Mecp2308 mutation. Hum. Mol. Genet. 2012, 21:2399-2411.
45. Yoo J.Y., Hurwitz B.S., Bolyard C., Yu J.G., Zhang J., Selvendiran K., Rath K.S., He S., Bailey Z., Eaves D., Cripe T.P., Parris D.S., Caligiuri M.A., Yu J., Old M., Kaur B. Bortezomib-induced unfolded protein response increases oncolytic HSV-1 replication resulting in synergistic antitumor effects. Clin. Cancer Res. 2014, 20:3787-3798.
46. Zhang Z.F., Fan S.H., Zheng Y.L., Lu J., Wu D.M., Shan Q., Hu B. Troxerutin protects the mouse liver against oxidative stress-mediated injury induced by d-galactose. J. Agric. Food Chem. 2009, 57:7731-7736.
47. Zhang Z.F., Fan S.H., Zheng Y.L., Lu J., Wu D.M., Shan Q., Hu B. Troxerutin improves hepatic lipid homeostasis by restoring NAD(+)-depletion-mediated dysfunction of lipin 1 signaling in high-fat diet-treated mice. Biochem. Pharmacol. 2014, 91:74-86.
48. Zhang Z.F., Zhang Y.Q., Fan S.H., Zhuang J., Zheng Y.L., Lu J., Wu D.M., Shan Q., Hu B. Troxerutin protects against 2,2',4,4'-tetrabromodiphenyl ether (BDE-47)-induced liver inflammation by attenuating oxidative stress-mediated NAD+-depletion. J. Hazard. Mater. 2015, 283:98-109.
49. Zheng Q.Y., Li P.P., Jin F.S., Yao C., Zhang G.H., Zang T., Ai X. Ursolic acid induces ER stress response to activate ASK1-JNK signaling and induce apoptosis in human bladder cancer T24 cells. Cell Signal. 2013, 25:206-213.