Curcumin attenuates quinocetone induced apoptosis and inflammation via the opposite modulation of Nrf2/HO-1 and NF-kB pathway in human hepatocyte L02 cells

Food and Chemical Toxicology

Volumn 95, Issue , 2016, Pages 52-63

  Dai, Chongshan ^a   Li, Bin ^a   Zhou, Yan ^a   Li, Daowen ^a   Zhang, Shen ^a   Li, Hui ^a   Xiao, Xilong ^a   Tang, Shusheng ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Apoptosis; Curcumin; Inflammatory response; NF kB pathway; Nrf2 HO 1 pathway; Quinocetone

Indexed keywords

CASPASE; CASPASE 3; CASPASE 9; CURCUMIN; HEME OXYGENASE 1; HISTONE DEACETYLASE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LACTATE DEHYDROGENASE; MESSENGER RNA; PROTOPORPHYRIN ZINC; QUINOXALINE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; NOS2 PROTEIN, HUMAN; QUINOCETONE; QUINOXALINE DERIVATIVE;

APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INFLAMMATION; LIVER CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATIVE STRESS; PROTEIN EXPRESSION; UPREGULATION; CELL CULTURE; CHEMICALLY INDUCED; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; CURCUMIN; HEME OXYGENASE-1; HEPATOCYTES; HUMANS; INFLAMMATION; L-LACTATE DEHYDROGENASE; NF-E2-RELATED FACTOR 2; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; QUINOXALINES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84977639449     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2016.06.025     Document Type: Article

References (60)

1. Barcelos, R.P., Bresciani, G., Rodriguez-Miguelez, P., Cuevas, M.J., Soares, F.A., Barbosa, N.V., Gonzalez-Gallego, J., Diclofenac pretreatment effects on the toll-like receptor 4/nuclear factor kappa B-mediated inflammatory response to eccentric exercise in rat liver. Life Sci. 148 (2016), 247–253.
2. Bellezza, I., Tucci, A., Galli, F., Grottelli, S., Mierla, A.L., Pilolli, F., Minelli, A., Inhibition of NF-kappaB nuclear translocation via HO-1 activation underlies alpha-tocopheryl succinate toxicity. J. Nutr. Biochem. 23 (2012), 1583–1591.
3. Chen, Q., Tang, S.S., Jin, X., Zou, J.J., Chen, K.P., Zhang, T., Xiao, X.L., Investigation of the genotoxicity of quinocetone, carbadox and olaquindox in vitro using Vero cells. Food Chem. Toxicol. 47 (2009), 328–334.
4. Cheng, G., Zhao, Y., Li, H., Wu, Y., Li, X., Han, Q., Dai, C., Li, Y., Forsythiaside attenuates lipopolysaccharide-induced inflammatory responses in the bursa of Fabricius of chickens by downregulating the NF-kappaB signaling pathway. Exp. Ther. Med. 7 (2014), 179–184.
5. Cuadrado, A., Martin-Moldes, Z., Ye, J., Lastres-Becker, I., Transcription factors NRF2 and NF-kappaB are coordinated effectors of the Rho family, GTP-binding protein RAC1 during inflammation. J. Biol. Chem. 289 (2014), 15244–15258.
6. Dai, C., Tang, S., Deng, S., Zhang, S., Zhou, Y., Velkov, T., Li, J., Xiao, X., Lycopene attenuates colistin-induced nephrotoxicity in mice via activation of the Nrf2/HO-1 pathway. Antimicrob. Agents Chemother. 59 (2015), 579–585.
7. Dai, C., Tang, S., Li, D., Zhao, K., Xiao, X., Curcumin attenuates quinocetone-induced oxidative stress and genotoxicity in human hepatocyte L02 cells. Toxicol. Mech. Methods 25 (2015), 340–346.
8. Dai, C., Tang, S., Velkov, T., Xiao, X., Colistin-induced apoptosis of neuroblastoma-2a cells involves the generation of reactive oxygen species, mitochondrial dysfunction, and autophagy. Mol. Neurobiol., 2015.
9. Dai, C., Zhang, D., Gao, R., Zhang, X., Li, J., Li, J., In vitro toxicity of colistin on primary chick cortex neurons and its potential mechanism. Environ. Toxicol. Pharmacol. 36 (2013), 659–666.
10. DiSilvestro, P.A., Ali, S., Craighead, P.S., Lucci, J.A., Lee, Y.C., Cohn, D.E., Spirtos, N.M., Tewari, K.S., Muller, C., Gajewski, W.H., Steinhoff, M.M., Monk, B.J., Phase III randomized trial of weekly cisplatin and irradiation versus cisplatin and tirapazamine and irradiation in stages IB2, IIA, IIB, IIIB, and IVA cervical carcinoma limited to the pelvis: a Gynecologic Oncology Group study. J. Clin. Oncol. 32 (2014), 458–464.
11. Elmore, S., Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35 (2007), 495–516.
12. Fang, J.J., Li, Y., Wu, S.M., Ma, K.P., Li, H.J., Gao, Z.X., Dong, F.T., Determination of quinocetone and its two major metabolites in chicken liver and muscle tissues by liquid chromatography-tandem mass spectrometry. Anal. Methods-Uk 4 (2012), 1149–1154.
13. Fattori, V., Pinho-Ribeiro, F.A., Borghi, S.M., Alves, J.C., Cunha, T.M., Cunha, F.Q., Casagrande, R., Verri, W.A., Curcumin inhibits superoxide anion-induced pain-like behavior and leukocyte recruitment by increasing Nrf2 expression and reducing NF-kappa B activation. Inflamm. Res. 64 (2015), 993–1003.
14. Gao, S., Duan, X., Wang, X., Dong, D., Liu, D., Li, X., Sun, G., Li, B., Curcumin attenuates arsenic-induced hepatic injuries and oxidative stress in experimental mice through activation of Nrf2 pathway, promotion of arsenic methylation and urinary excretion. Food Chem. Toxicol. 59 (2013), 739–747.
15. Ghattass, K., El-Sitt, S., Zibara, K., Rayes, S., Haddadin, M.J., El-Sabban, M., Gali-Muhtasib, H., The quinoxaline di-N-oxide DCQ blocks breast cancer metastasis in vitro and in vivo by targeting the hypoxia inducible factor-1 pathway. Mol. Cancer, 13, 2014.
16. Ghosh, S., Banerjee, S., Sil, P.C., The beneficial role of curcumin on inflammation, diabetes and neurodegenerative disease: a recent update. Food Chem. Toxicol. 83 (2015), 111–124.
17. He, L., Peng, X., Zhu, J., Liu, G., Chen, X., Tang, C., Liu, H., Liu, F., Peng, Y., Protective effects of curcumin on acute gentamicin-induced nephrotoxicity in rats. Can. J. Physiol. Pharmacol. 93 (2015), 275–282.
18. Hoesel, B., Schmid, J.A., The complexity of NF-kappaB signaling in inflammation and cancer. Mol. Cancer, 12, 2013, 86.
19. Ihsan, A., Wang, X., Zhang, W., Tu, H.G., Wang, Y.L., Huang, L.L., Iqbal, Z., Cheng, G.Y., Pan, Y.H., Liu, Z.L., Tan, Z.Q., Zhang, Y.Y., Yuan, Z.H., Genotoxicity of quinocetone, cyadox and olaquindox in vitro and in vivo. Food Chem. Toxicol. 59 (2013), 207–214.
20. Khosravi-Far, R., Esposti, M.D., Death receptor signals to mitochondria. Cancer Biol. Ther. 3 (2004), 1051–1057.
21. Lee, J., Kang, U., Seo, E.K., Kim, Y.S., Heme oxygenase-1-mediated anti-inflammatory effects of tussilagonone on macrophages and 12-O-tetradecanoylphorbol-13-acetate-induced skin inflammation in mice. Int. Immunopharmacol. 34 (2016), 155–164.
22. Li, J.Y., Li, J.S., Xu, Z.Z., Lu, R.H., HPLC determination of quinocetone in edible chicken tissues. Toxicology, 191, 2003 55–55.
23. Li, W., Suwanwela, N.C., Patumraj, S., Curcumin by down regulating NF-kB and elevating Nrf2, reduces brain edema and neurological dysfunction after cerebral I/R. Microvasc. Res. 106 (2016), 117–127.
24. Liu, G.H., Qu, J., Shen, X., NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim. Biophys. Acta 1783 (2008), 713–727.
25. Liu, Q., Zhang, J., Luo, X., Ihsan, A., Liu, X., Dai, M., Cheng, G., Hao, H., Wang, X., Yuan, Z., Further investigations into the genotoxicity of quinoxaline-di-N-oxides and their primary metabolites. Food Chem. Toxicol. 93 (2016), 145–157.
26. Maluf, S.W., Marroni, N.P., Heuser, V.D., Pra, D., DNA damage and oxidative stress in human disease. Biomed. Res. Int., 2013, 2013, 696104.
27. Pang, C., Zheng, Z., Shi, L., Sheng, Y., Wei, H., Wang, Z., Ji, L., Caffeic acid prevents acetaminophen-induced liver injury by activating the Keap1-Nrf2 antioxidative defense system. Free Radic. Biol. Med. 91 (2016), 236–246.
28. Shen, J.Z., Yang, C.Y., Wu, C.M., Feng, P.S., Wang, Z.H., Li, Y., Li, Y.S., Zhang, S.X., Identification of the major metabolites of quinocetone in swine urine using ultra-performance liquid chromatography/electrospray ionization quadrupole time-of-flight tandem mass spectrometry. Rapid Commun. Mass Sp. 24 (2010), 375–383.
29. Snyder, C.M., Shroff, E.H., Liu, J., Chandel, N.S., Nitric oxide induces cell death by regulating anti-apoptotic BCL-2 family members. PLoS One, 4, 2009, e7059.
30. Soto-Urquieta, M.G., Lopez-Briones, S., Perez-Vazquez, V., Saavedra-Molina, A., Gonzalez-Hernandez, G.A., Ramirez-Emiliano, J., Curcumin restores mitochondrial functions and decreases lipid peroxidation in liver and kidneys of diabetic db/db mice. Biol. Res., 47, 2014, 74.
31. Tait, S.W., Green, D.R., Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11 (2010), 621–632.
32. Vicente, E., Villar, R., Perez-Silanes, S., Aldana, I., Goldman, R.C., Mong, A., Quinoxaline 1,4-di-N-oxide and the potential for treating tuberculosis. Infect. Disord. Drug Targets 11 (2011), 196–204.
33. Vieira, M., Pinheiro, C., Fernandes, R., Noronha, J.P., Prudencio, C., Antimicrobial activity of quinoxaline 1,4-dioxide with 2-and 3-substituted derivatives. Microbiol. Res. 169 (2014), 287–293.
34. Wang, D., Luo, X., Zhong, Y., Yang, W., Xu, M., Liu, Y., Meng, J., Yao, P., Yan, H., Liu, L., Pu-erh black tea extract supplementation attenuates the oxidative DNA damage and oxidative stress in Sprague-Dawley rats with renal dysfunction induced by subchronic 3-methyl-2-quinoxalin benzenevinylketo-1,4-dioxide exposure. Food Chem. Toxicol. 50 (2012), 147–154.
35. Wang, D., Zhong, Y., Luo, X., Wu, S., Xiao, R., Bao, W., Yang, W., Yan, H., Yao, P., Liu, L., Pu-erh black tea supplementation decreases quinocetone-induced ROS generation and oxidative DNA damage in Balb/c mice. Food Chem. Toxicol. 49 (2011), 477–484.
36. Wang, D., Zhong, Y., Luo, X.A., Wu, S.A., Xiao, R., Bao, W., Yang, W., Yan, H., Yao, P., Liu, L.G., Pu-erh black tea supplementation decreases quinocetone-induced ROS generation and oxidative DNA damage in Balb/c mice. Food Chem. Toxicol. 49 (2011), 477–484.
37. Wang, H., Liu, H., Zheng, Z.M., Zhang, K.B., Wang, T.P., Sribastav, S.S., Liu, W.S., Liu, T., Role of death receptor, mitochondrial and endoplasmic reticulum pathways in different stages of degenerative human lumbar disc. Apoptosis 16 (2011), 990–1003.
38. Wang, X., Wan, D., Ihsan, A., Liu, Q., Cheng, G., Li, J., Liu, Z., Yuan, Z., Mechanism of adrenocortical toxicity induced by quinocetone and its bidesoxy-quinocetone metabolite in porcine adrenocortical cells in vitro. Food Chem. Toxicol. 84 (2015), 115–124.
39. Wang, X., Zhang, H., Huang, L., Pan, Y., Li, J., Chen, D., Cheng, G., Hao, H., Tao, Y., Liu, Z., Yuan, Z., Deoxidation rates play a critical role in DNA damage mediated by important synthetic drugs, quinoxaline 1,4-dioxides. Chem. Res. Toxicol. 28 (2015), 470–481.
40. Wang, X., Zhang, W., Wang, Y., Peng, D., Ihsan, A., Huang, X., Huang, L., Liu, Z., Dai, M., Zhou, W., Yuan, Z.H., Acute and sub-chronic oral toxicological evaluations of quinocetone in Wistar rats. Regul. Toxicol. Pharmacol. 58 (2010), 421–427.
41. Wang, X., Zhang, W., Wang, Y.L., Ihsan, A., Dai, M.H., Huang, L.L., Chen, D.M., Tao, Y.F., Peng, D.P., Liu, Z.L., Yuan, Z.H., Two generation reproduction and teratogenicity studies of feeding quinocetone fed to Wistar rats. Food Chem. Toxicol. 50 (2012), 1600–1609.
42. Wang, X., Zhou, W., Ihsan, A., Chen, D.M., Cheng, G.Y., Hao, H.H., Liu, Z.L., Wang, Y.L., Yuan, Z.H., Assessment of thirteen-week subchronic oral toxicity of cyadox in Beagle dogs. Regul. Toxicol. Pharm. 73 (2015), 652–659.
43. Waseem, M., Parvez, S., Neuroprotective activities of curcumin and quercetin with potential relevance to mitochondrial dysfunction induced by oxaliplatin. Protoplasma 253 (2016), 417–430.
44. Xing, H.Y., Liu, Y., Chen, J.H., Sun, F.J., Shi, H.Q., Xia, P.Y., Hyperoside attenuates hydrogen peroxide-induced L02 cell damage via MAPK-dependent Keap₁-Nrf₂-ARE signaling pathway. Biochem. Biophys. Res. Commun. 410 (2011), 759–765.
45. Xiong, Z.E., Dong, W.G., Wang, B.Y., Tong, Q.Y., Li, Z.Y., Curcumin attenuates chronic ethanol-induced liver injury by inhibition of oxidative stress via mitogen-activated protein kinase/nuclear factor E2-related factor 2 pathway in mice. Pharmacogn. Mag. 11 (2015), 707–715.
46. Yamashita, Y., Ueyama, T., Nishi, T., Yamamoto, Y., Kawakoshi, A., Sunami, S., Iguchi, M., Tamai, H., Ueda, K., Ito, T., Tsuruo, Y., Ichinose, M., Nrf2-inducing anti-oxidation stress response in the rat liver–new beneficial effect of lansoprazole. PLoS One, 9, 2014, e97419.
47. Yang, W., Fu, J., Xiao, X., Yan, H., Bao, W., Wang, D., Hao, L.P., Nussler, A.K., Yao, P., Liu, L.G., Quinocetone triggers oxidative stress andinduces cytotoxicity and genotoxicity inhuman peripheral lymphocytes of both genders. J. Sci. Food Agric. 93 (2013), 1317–1325.
48. Yu, M., Wang, D., Xu, M., Liu, Y., Wang, X., Liu, J., Yang, X., Yao, P., Yan, H., Liu, L., Quinocetone-induced Nrf2/HO-1 pathway suppression aggravates hepatocyte damage of Sprague-Dawley rats. Food Chem. Toxicol. 69 (2014), 210–219.
49. Yu, M., Wang, D., Xu, M.J., Liu, Y., Wang, X., Liu, J., Yang, X.F., Yao, P., Yan, H., Liu, L.G., Quinocetone-induced Nrf2/HO-1 pathway suppression aggravates hepatocyte damage of Sprague-Dawley rats. Food Chem. Toxicol. 69 (2014), 210–219.
50. Yu, M., Wang, D., Yang, W., Xu, M.J., Liu, Y., Xu, S.Y., Yao, P., Yan, H., Liu, L.G., Mechanisms of Nrf2/HO-1 pathway up-regulation induced by pu-erh black tea extract supplementation for quinocetone-treated Sprague-Dawley rats. J. Funct. Foods 14 (2015), 767–778.
51. Yu, M., Xu, M., Liu, Y., Yang, W., Rong, Y., Yao, P., Yan, H., Wang, D., Liu, L., Nrf2/ARE is the potential pathway to protect Sprague-Dawley rats against oxidative stress induced by quinocetone. Regul. Toxicol. Pharmacol. 66 (2013), 279–285.
52. Yu, M., Xu, M.J., Liu, Y., Yang, W., Rong, Y., Yao, P., Yan, H., Wang, D., Liu, L.G., Nrf2/ARE is the potential pathway to protect Sprague-Dawley rats against oxidative stress induced by quinocetone. Regul. Toxicol. Pharm. 66 (2013), 279–285.
53. Zeng, C., Zhong, P., Zhao, Y., Kanchana, K., Zhang, Y., Khan, Z.A., Chakrabarti, S., Wu, L., Wang, J., Liang, G., Curcumin protects hearts from FFA-induced injury by activating Nrf2 and inactivating NF-kappaB both in vitro and in vivo. J. Mol. Cell Cardiol. 79 (2015), 1–12.
54. Zhang, C., Wang, C., Tang, S., Sun, Y., Zhao, D., Zhang, S., Deng, S., Zhou, Y., Xiao, X., TNFR1/TNF-alpha and mitochondria interrelated signaling pathway mediates quinocetone-induced apoptosis in HepG2 cells. Food Chem. Toxicol. 62 (2013), 825–838.
55. Zhang, K., Wang, X., Wang, C., Zheng, H., Li, T., Xiao, S., Wang, M., Fei, C., Zhang, L., Xue, F., Investigation of quinocetone-induced mitochondrial damage and apoptosis in HepG2 cells and compared with its metabolites. Environ. Toxicol. Pharmacol. 39 (2015), 555–567.
56. Zhang, K.Y., Wang, X.Y., Wang, C.M., Zheng, H.H., Li, T., Xiao, S., Wang, M., Fei, C.Z., Zhang, L.F., Xue, F.Q., Investigation of quinocetone-induced mitochondrial damage and apoptosis in HepG2 cells and compared with its metabolites. Environ. Toxicol. Phar. 39 (2015), 555–567.
57. Zhang, K.Y., Zheng, W.L., Zheng, H.H., Wang, C.M., Wang, M., Li, T., Wang, X.Y., Zhang, L.F., Xiao, S., Fei, C.Z., Xue, F.Q., Identification of oxidative stress and responsive genes of HepG2 cells exposed to quinocetone, and compared with its metabolites. Cell Biol. Toxicol. 30 (2014), 313–329.
58. Zhong, J.L., Zhang, G.J., Shen, X.G., Wang, L., Fang, B.H., Ding, H.Z., Pharmacokinetics of quinocetone and its major metabolites in swine after intravenous and oral administration. Agric. Sci. China 10 (2011), 1292–1300.
59. Zoja, C., Benigni, A., Remuzzi, G., The Nrf2 pathway in the progression of renal disease. Nephrol. Dial. Transpl. 29:Suppl. l (2014), i19–i24.
60. Zou, J.J., Chen, Q., Jin, X., Tang, S.S., Chen, K.P., Zhang, T., Xiao, X.L., Olaquindox induces apoptosis through the mitochondrial pathway in HepG2 cells. Toxicology 285 (2011), 104–113.