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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 3631565, 14 pages
https://doi.org/10.1155/2017/3631565
Research Article

Hepatoprotective Effect of Polyphenol-Enriched Fraction from Folium Microcos on Oxidative Stress and Apoptosis in Acetaminophen-Induced Liver Injury in Mice

1Application Technique Engineering Center of Natural Cosmeceuticals, College of Fuijan Province, Xiamen Medical College, Xiamen, Fujian 361023, China
2Research Center of Natural Cosmeceuticals Engineering, Xiamen Medical College, Xiamen, Fujian 361023, China
3Fujian Provincial Key Laboratory of Biological Engineering on Traditional Herbs, Xiamen Medical College, Xiamen, Fujian 361023, China
4Technology and Engineering Center for Marine Biomedical Resource Utilization, Xiamen Medical College, Xiamen, Fujian 361023, China
5Department of Pharmacy, Xiamen Medical College, Xiamen, Fujian 361023, China

Correspondence should be addressed to Gang Zhang; nc.ude.cmmx@gz and Gueyhorng Wang; nc.ude.cmmx@hgw

Received 21 November 2016; Revised 24 February 2017; Accepted 20 March 2017; Published 23 May 2017

Academic Editor: Jie Li

Copyright © 2017 Hongtan Wu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. Yan, Q. Y. Zhang, L. Jiao et al., “Synergistic hepatoprotective effect of Schisandrae lignans with Astragalus polysaccharides on chronic liver injury in rats,” Phytomedicine, vol. 16, no. 9, pp. 805–813, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Jaeschke, G. J. Gores, A. I. Cederbaum, J. A. Hinson, D. Pessayre, and J. J. Lemasters, “Mechanisms of hepatotoxicity,” Toxicological Sciences, vol. 65, no. 2, pp. 166–176, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. S. H. Chan, M. H. Tai, C. Y. Li, and J. Y. Chan, “Reduction in molecular synthesis or enzyme activity of superoxide dismutases and catalase contributes to oxidative stress and neurogenic hypertension in spontaneously hypertensive rats,” Free Radical Biology & Medicine, vol. 40, no. 11, pp. 2028–2039, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Zhu, Y. Wang, L. Zhang, and Q. Guo, “Oxidative stress and liver disease,” Hepatology Research, vol. 42, no. 8, pp. 741–749, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. A. M. Larson, J. Polson, R. J. Fontana et al., “Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study,” Hepatology, vol. 42, no. 6, pp. 1364–1372, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. R. N. Jadeja, N. H. Urrunaga, S. Dash, S. Khurana, and N. K. Saxena, “Withaferin-A reduces acetaminophen-induced liver injury in mice,” Biochemical Pharmacology, vol. 97, no. 1, pp. 122–132, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Song, J. Fu, X. Xia, C. Su, and Y. Song, “Bazhen decoction protects against acetaminophen induced acute liver injury by inhibiting oxidative stress, inflammation and apoptosis in mice,” PLoS One, vol. 9, no. 9, article e107405, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Tian, X. Shi, L. Yu, J. Zhu, R. Ma, and X. Yang, “Chemical composition and hepatoprotective effects of polyphenol-rich extract from Houttuynia cordata tea,” Journal of Agricultural and Food Chemistry, vol. 60, no. 18, pp. 4641–4648, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Saberi, M. D. Ybanez, H. S. Johnson, W. A. Gaarde, D. Han, and N. Kaplowitz, “Protein kinase C (PKC) participates in acetaminophen hepatotoxicity through c-jun-N-terminal kinase (JNK)-dependent and -independent signaling pathways,” Hepatology, vol. 59, no. 4, pp. 1543–1554, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Ding, Q. Li, Y. Xu et al., “Attenuating oxidative stress by paeonol protected against acetaminophen-induced hepatotoxicity in mice,” PLoS One, vol. 11, no. 5, article e0154375, 2016. View at Publisher · View at Google Scholar
  11. H. Schroeter, C. S. Boyd, R. Ahmed et al., “c-Jun N-terminal kinase (JNK)-mediated modulation of brain mitochondria function: new target proteins for JNK signalling in mitochondrion-dependent apoptosis,” The Biochemical Journal, vol. 372, no. Part 2, pp. 359–369, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. W. Wang, C. Guan, X. Sun et al., “Tanshinone IIA protects against acetaminophen-induced hepatotoxicity via activating the Nrf2 pathway,” Phytomedicine, vol. 23, no. 6, pp. 589–596, 2016. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. M. Jiang, Y. Wang, H. S. Tan et al., “Schisandrol B protects against acetaminophen-induced acute hepatotoxicity in mice via activation of the NRF2/ARE signaling pathway,” Acta Pharmacologica Sinica, vol. 37, no. 3, pp. 382–389, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. L. M. Aleksunes, A. L. Slitt, J. M. Maher et al., “Induction of Mrp3 and Mrp4 transporters during acetaminophen hepatotoxicity is dependent on Nrf2,” Toxicology and Applied Pharmacology, vol. 226, no. 1, pp. 74–83, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Enomoto, K. Itoh, E. Nagayoshi et al., “High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes,” Toxicological Sciences, vol. 59, no. 1, pp. 169–177, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Chan, X. D. Han, and Y. W. Kan, “An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 8, pp. 4611–4616, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Okawa, H. Motohashi, A. Kobayashi, H. Aburatani, T. W. Kensler, and M. Yamamoto, “Hepatocyte-specific deletion of the keap1 gene activates Nrf2 and confers potent resistance against acute drug toxicity,” Biochemical and Biophysical Research Communications, vol. 339, no. 1, pp. 79–88, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. O. Ulicna, M. Greksak, O. Vancova et al., “Hepatoprotective effect of rooibos tea (Aspalathus linearis) on CCl4-induced liver damage in rats,” Physiological Research, vol. 52, no. 4, pp. 461–466, 2003. View at Google Scholar
  19. E. Joubert, E. S. Richards, J. D. Merwe, D. De Beer, M. Manley, and W. C. Gelderblom, “Effect of species variation and processing on phenolic composition and in vitro antioxidant activity of aqueous extracts of Cyclopia spp. (Honeybush Tea),” Journal of Agricultural and Food Chemistry, vol. 56, no. 3, pp. 954–963, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Paul, M. A. Islam, E. M. Tanvir et al., “Satkara (Citrus macroptera) fruit protects against acetaminophen-induced hepatorenal toxicity in rats,” Evidence-Based Complementary and Alternative Medicine, vol. 2016, Article ID 9470954, p. 11, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. P. C. Still, B. Yi, T. F. Gonzalez-Cestari et al., “Alkaloids from Microcos paniculata with cytotoxic and nicotinic receptor antagonistic activities,” Journal of Natural Products, vol. 76, no. 2, pp. 243–249, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. G. Chen, P. Li, R. Yan et al., “Alpha-glucosidase inhibitory effect and simultaneous quantification of three major flavonoid glycosides in Microctis folium,” Molecules, vol. 18, no. 4, pp. 4221–4232, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. S. X. Feng, L. D. Lin, H. H. Xu, and X. Y. Wei, “Two new piperidine alkaloids from the leaves of Microcos paniculata,” Journal of Asian Natural Products Research, vol. 10, no. 11-12, pp. 1155–1158, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Itoh and Y. Furuichi, “Lowering serum cholesterol level by feeding a 40% ethanol-eluted fraction from HP-20 resin treated with hot water extract of adzuki beans (Vigna angularis) to rats fed a high-fat cholesterol diet,” Nutrition, vol. 25, no. 3, pp. 318–321, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. V. L. Singleton and J. A. Rossi, “Colorimetry of total phenolics with phosphomolybdic-phosphotungstic asit reagents,” American Journal of Enology and Viticulture, vol. 16, no. 3, pp. 144–158, 1965. View at Google Scholar
  26. J. Zhishen, T. Mengcheng, and W. Jianming, “The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals,” Food Chemistry, vol. 64, no. 4, pp. 555–559, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Zhu, H. Zhou, and H. Qian, “Antioxidant and free radical-scavenging activities of wheat germ protein hydrolysates (WGPH) prepared with alcalase,” Process Biochemistry, vol. 41, no. 6, pp. 1296–1302, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Nishikimi, N. A. Rao, and K. Yagi, “The occurrence of superoxide anion in the reaction of reduced phenazine methosulphate and molecular oxygen,” Biochemical and Biophysical Research Communications, vol. 46, no. 2, pp. 849–854, 1972. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Guo, S. Liu, P. Dong et al., “Akbu-LAAO exhibits potent anti-tumor activity to HepG2 cells partially through produced H2O2 via TGF-beta signal pathway,” Scientific Reports, vol. 5, p. 18215, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. M. B. Hansen, S. E. Nielsen, and K. Berg, “Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill,” Journal of Immunological Methods, vol. 119, no. 2, pp. 203–210, 1989. View at Publisher · View at Google Scholar · View at Scopus
  31. L. Liu, H. Xie, X. Chen et al., “Differential response of normal human epidermal keratinocytes and HaCaT cells to hydrogen peroxide-induced oxidative stress,” Clinical and Experimental Dermatology, vol. 37, no. 7, pp. 772–780, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Shimoda, J. Tanaka, M. Kikuchi et al., “Walnut polyphenols prevent liver damage induced by carbon tetrachloride and δ-galactosamine: hepatoprotective hydrolyzable tannins in the kernel pellicles of walnut,” Journal of Agricultural and Food Chemistry, vol. 56, no. 12, pp. 4444–4449, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. V. M. Moo-Huchin, M. I. Moo-Huchin, R. J. Estrada-Leon et al., “Antioxidant compounds, antioxidant activity and phenolic content in peel from three tropical fruits from Yucatan, Mexico,” Food Chemistry, vol. 166, pp. 17–22, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. M. R. McGill, C. D. Williams, Y. Xie, A. Ramachandran, and H. Jaeschke, “Acetaminophen-induced liver injury in rats and mice: comparison of protein adducts, mitochondrial dysfunction, and oxidative stress in the mechanism of toxicity,” Toxicology and Applied Pharmacology, vol. 264, no. 3, pp. 387–394, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. X. Yang, C. Dong, and G. Ren, “Effect of soyasaponins-rich extract from soybean on acute alcohol-induced hepatotoxicity in mice,” Journal of Agricultural and Food Chemistry, vol. 59, no. 4, pp. 1138–1144, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. G. E. Kass, P. Macanas-Pirard, P. C. Lee, and R. H. Hinton, “The role of apoptosis in acetaminophen-induced injury,” Annals of the new York Academy of Sciences, vol. 1010, no. 1, pp. 557–559, 2003. View at Google Scholar
  37. B. Hu and L. M. Colletti, “CXC receptor-2 knockout genotype increases X-linked inhibitor of apoptosis protein and protects mice from acetaminophen hepatotoxicity,” Hepatology, vol. 52, no. 2, pp. 691–702, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Latchoumycandane, C. W. Goh, M. M. Ong, and U. A. Boelsterli, “Mitochondrial protection by the JNK inhibitor leflunomide rescues mice from acetaminophen-induced liver injury,” Hepatology, vol. 45, no. 2, pp. 412–421, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Jaeschke, M. R. McGill, C. D. Williams, and A. Ramachandran, “Current issues with acetaminophen hepatotoxicity—a clinically relevant model to test the efficacy of natural products,” Life Sciences, vol. 88, no. 17-18, pp. 737–745, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. K. J. Heard, “Acetylcysteine for acetaminophen poisoning,” The New England Journal of Medicine, vol. 359, no. 3, pp. 285–292, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. E. A. Sandilands and D. N. Bateman, “Adverse reactions associated with acetylcysteine,” Clinical Toxicology (Philadelphia, Pa.), vol. 47, no. 2, pp. 81–88, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. A. S. Darvesh, R. T. Carroll, A. Bishayee, W. J. Geldenhuys, and C. J. Van der Schyf, “Oxidative stress and Alzheimer's disease: dietary polyphenols as potential therapeutic agents,” Expert Review of Neurotherapeutics, vol. 10, no. 5, pp. 729–745, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Hanawa, M. Shinohara, B. Saberi, W. A. Gaarde, D. Han, and N. Kaplowitz, “Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury,” The Journal of Biological Chemistry, vol. 283, no. 20, pp. 13565–13577, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. B. K. Gunawan, Z. X. Liu, D. Han, N. Hanawa, W. A. Gaarde, and N. Kaplowitz, “c-Jun N-terminal kinase plays a major role in murine acetaminophen hepatotoxicity,” Gastroenterology, vol. 131, no. 1, pp. 165–178, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Kumari and P. Kakkar, “Lupeol prevents acetaminophen-induced in vivo hepatotoxicity by altering the Bax/Bcl-2 and oxidative stress-mediated mitochondrial signaling cascade,” Life Sciences, vol. 90, no. 15-16, pp. 561–570, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Dong, L. Xu, X. Han et al., “Effects of the total saponins from Rosa laevigata Michx fruit against acetaminophen-induced liver damage in mice via induction of autophagy and suppression of inflammation and apoptosis,” Molecules, vol. 19, no. 6, pp. 7189–7206, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. Q. Ma and X. He, “Molecular basis of electrophilic and oxidative defense: promises and perils of Nrf2,” Pharmacological Reviews, vol. 64, no. 4, pp. 1055–1081, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. J. S. Moffit, L. M. Aleksunes, M. J. Kardas, A. L. Slitt, C. D. Klaassen, and J. E. Manautou, “Role of NAD(P)H:quinone oxidoreductase 1 in clofibrate-mediated hepatoprotection from acetaminophen,” Toxicology, vol. 230, no. 2-3, pp. 197–206, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. N. G. Abraham and A. Kappas, “Pharmacological and clinical aspects of heme oxygenase,” Pharmacological Reviews, vol. 60, no. 1, pp. 79–127, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. J. H. Yang, B. Y. Shin, J. Y. Han et al., “Isorhamnetin protects against oxidative stress by activating Nrf2 and inducing the expression of its target genes,” Toxicology and Applied Pharmacology, vol. 274, no. 2, pp. 293–301, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. G. Z. Dong, J. H. Lee, S. H. Ki et al., “AMPK activation by isorhamnetin protects hepatocytes against oxidative stress and mitochondrial dysfunction,” European Journal of Pharmacology, vol. 740, pp. 634–640, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. J. H. Yang, S. C. Kim, K. M. Kim et al., “Isorhamnetin attenuates liver fibrosis by inhibiting TGF-beta/Smad signaling and relieving oxidative stress,” European Journal of Pharmacology, vol. 783, pp. 92–102, 2016. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Gevrenova, M. Kondeva-Burdina, N. Denkov, and D. Zheleva-Dimitrova, “Flavonoid profiles of three Bupleurum species and in vitro hepatoprotective of activity Bupleurum flavum Forsk,” Pharmacognosy Magazine, vol. 11, no. 41, pp. 14–23, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. J. M. Hur, S. H. Park, J. W. Choi, and J. C. Park, “Effects of extract and isorhamnetin glycoside from Brassica juncea on hepatic alcohol-metabolizing enzyme system in rats,” Natural Product Sciences, vol. 18, no. 3, pp. 190–194, 2012. View at Google Scholar
  55. T. Liu, X. H. Yu, E. Z. Gao et al., “Hepatoprotective effect of active constituents isolated from mung beans (Phaseolus radiatus L.) in an alcohol-induced liver injury mouse model,” Journal of Food Biochemistry, vol. 38, no. 5, pp. 453–459, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. J. H. Kim, B. C. Lee, G. S. Sim et al., “The isolation and antioxidative effects of vitexin from Acer palmatum,” Archives of Pharmacal Research, vol. 28, no. 2, pp. 195–202, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. C. M. Lin, C. T. Chen, H. H. Lee, and J. K. Lin, “Prevention of cellular ROS damage by isovitexin and related flavonoids,” Planta Medica, vol. 68, no. 4, pp. 365–367, 2002. View at Publisher · View at Google Scholar · View at Scopus