Table of Contents Author Guidelines Submit a Manuscript
Evidence-Based Complementary and Alternative Medicine
Volume 2018, Article ID 3140267, 11 pages
https://doi.org/10.1155/2018/3140267
Research Article

Zanthoxylum ailanthoides Suppresses Oleic Acid-Induced Lipid Accumulation through an Activation of LKB1/AMPK Pathway in HepG2 Cells

1Korea Research Institute of Bioscience and Biotechnology (KRIBB), Cheongju, Chungbuk 28116, Republic of Korea
2College of Pharmacy, Chungbuk National University, Cheongju, Chungbuk 28644, Republic of Korea
3Department of Biology Education, Daegu University, Gyeongsan-si, Gyeongsangbuk 38453, Republic of Korea

Correspondence should be addressed to Dong-Oh Moon; rk.ca.ugead@noomod, Hyun-Sun Lee; rk.er.bbirk@sheel, and Mun-Ock Kim; rk.er.bbirk@mikom

Received 4 September 2017; Revised 1 November 2017; Accepted 27 November 2017; Published 8 January 2018

Academic Editor: Shao-Hsuan Kao

Copyright © 2018 Eun-Bin Kwon 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. J. M. Schattenberg and D. Schuppan, “Nonalcoholic steatohepatitis: The therapeutic challenge of a global epidemic,” Current Opinion in Lipidology, vol. 22, no. 6, pp. 479–488, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Katsiki, D. P. Mikhailidis, and C. S. Mantzoros, “Non-alcoholic fatty liver disease and dyslipidemia: An update,” Metabolism - Clinical and Experimental, vol. 65, no. 8, pp. 1109–1123, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Cusi, “Treatment of patients with type 2 diabetes and non-alcoholic fatty liver disease: current approaches and future directions,” Diabetologia, vol. 59, no. 6, pp. 1112–1120, 2016. View at Publisher · View at Google Scholar
  4. P. Tessari, A. Coracina, A. Cosma, and A. Tiengo, “Hepatic lipid metabolism and non-alcoholic fatty liver disease,” Nutrition, Metabolism & Cardiovascular Diseases, vol. 19, no. 4, pp. 291–302, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. B. B. Kahn, T. Alquier, D. Carling, and D. G. Hardie, “AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism,” Cell Metabolism, vol. 1, no. 1, pp. 15–25, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Viollet, S. Horman, J. Leclerc et al., “AMPK inhibition in health and disease,” Critical Reviews in Biochemistry and Molecular Biology, vol. 45, no. 4, pp. 276–295, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Viollet, B. Guigas, J. Leclerc et al., “AMP-activated protein kinase in the regulation of hepatic energy metabolism: From physiology to therapeutic perspectives,” Acta Physiologica, vol. 196, no. 1, pp. 81–98, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Wang, N. Moustaid-Moussa, L. Chen et al., “Novel insights of dietary polyphenols and obesity,” The Journal of Nutritional Biochemistry, vol. 25, no. 1, pp. 1–18, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. G. Zhou, R. Myers, Y. Li et al., “Role of AMP-activated protein kinase in mechanism of metformin action,” The Journal of Clinical Investigation, vol. 108, no. 8, pp. 1167–1174, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. C.-Y. Chung, T.-L. Hwang, L.-M. Kuo et al., “New benzo[c]phenanthridine and benzenoid derivatives, and other constituents from Zanthoxylum ailanthoides: Effects on neutrophil pro-inflammatory responses,” International Journal of Molecular Sciences, vol. 14, no. 11, pp. 22395–22408, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Hsiao, C.-Y. Chang, M.-Y. Shen et al., “α-Naphthoflavone, a potent antiplatelet flavonoid, is mediated through inhibition of phospholipase C activity and stimulation of cyclic GMP formation,” Journal of Agricultural and Food Chemistry, vol. 53, no. 13, pp. 5179–5186, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. J.-J. Chen, C.-Y. Chung, T.-L. Hwang, and J.-F. Chen, “Amides and benzenoids from Zanthoxylum ailanthoides with inhibitory activity on superoxide generation and elastase release by neutrophils,” Journal of Natural Products, vol. 72, no. 1, pp. 107–111, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. C.-Y. Chu, H.-J. Lee, C.-Y. Chu, Y.-F. Yin, and T.-H. Tseng, “Protective effects of leaf extract of Zanthoxylum ailanthoides on oxidation of low-density lipoprotein and accumulation of lipid in differentiated THP-1 cells,” Food and Chemical Toxicology, vol. 47, no. 6, pp. 1265–1271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. S. T. Chou, H. Y. Peng, C. T. Chang et al., “Zanthoxylum ailanthoides Sieb and Zucc. extract inhibits growth and induces cell death through G2/M-phase arrest and activation of apoptotic signals in colo 205 human colon adenocarcinoma cells,” Anticancer Reseach, vol. 31, no. 5, pp. 1667–1676, 2011. View at Google Scholar · View at Scopus
  15. S.-T. Chou, H.-H. Chan, H.-Y. Peng, M.-J. Liou, and T.-S. Wu, “Isolation of substances with antiproliferative and apoptosis-inducing activities against leukemia cells from the leaves of Zanthoxylum ailanthoides Sieb. & Zucc,” Phytomedicine, vol. 18, no. 5, pp. 344–348, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. H. J. Kim, J.-G. Jun, and J.-K. Kim, “2-(4-hydroxyphenyl)-5-(3-hydroxypropenyl)-7-methoxybenzofuran, a novel ailanthoidol derivative, exerts anti-inflammatory effect through downregulation of mitogen-activated protein kinase in lipopolysaccharide-treated RAW 264.7 cells,” Korean Journal of Physiology & Pharmacology, vol. 17, no. 3, pp. 217–222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Bullon, H. N. Newman, and M. Battino, “Obesity, diabetes mellitus, atherosclerosis and chronic periodontitis: a shared pathology via oxidative stress and mitochondrial dysfunction?” Periodontology 2000, vol. 64, no. 1, pp. 139–153, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. M.-S. Lee, J.-S. Kim, S.-M. Cho, S. O. Lee, S.-H. Kim, and H.-J. Lee, “Fermented Rhus verniciflua Stokes Extract Exerts an Antihepatic Lipogenic Effect in Oleic-Acid-Induced HepG2 Cells via Upregulation of AMP-Activated Protein Kinase,” Journal of Agricultural and Food Chemistry, vol. 63, no. 32, pp. 7270–7276, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. J.-H. Kim, S.-I. Kang, H.-S. Shin et al., “Sasa quelpaertensis and p-coumaric acid attenuate oleic acid-induced lipid accumulation in HepG2 cells,” Bioscience, Biotechnology, and Biochemistry, vol. 77, no. 7, pp. 1595–1598, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. M. F. Rodrigues Graciano, M. M. R. Valle, A. Kowluru, R. Curi, and A. R. Carpinelli, “Regulation of insulin secretion and production of reactive oxygen species by free fatty acids in pancreatic islets,” Islets, vol. 3, no. 5, pp. 213–223, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. A. M. Gusdon, K.-X. Song, and S. Qu, “Nonalcoholic fatty liver disease: pathogenesis and therapeutics from a mitochondria-centric perspective,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 637027, 20 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Y. Han, “Roles of reactive oxygen species on insulin resistance in adipose tissue,” Diabetes & Metabolism, vol. 40, no. 4, pp. 272–279, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. M. G. Macey, J. Sangster, P. A. Veys, and A. C. Newland, “Flow cytometric analysis of the functional ability of neutrophils from patients with autoimmune neutropenia,” Journal of Microscopy, vol. 159, no. 3, pp. 277–283, 1990. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Garcia-Ruiz, C. Rodriguez-Juan, T. Diaz-Sanjuan et al., “Uric acid and anti-TNF antibody improve mitochondrial dysfunction in ob/ob mice,” Hepatology, vol. 44, no. 3, pp. 581–591, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Schimmack, R. A. DeFronzo, and N. Musi, “AMP-activated protein kinase: role in metabolism and therapeutic implications,” Diabetes, Obesity and Metabolism, vol. 8, no. 6, pp. 591–602, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. D. G. Hardie, “AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy,” Nature Reviews Molecular Cell Biology, vol. 8, no. 10, pp. 774–785, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Grahame Hardie and M. L. J. Ashford, “AMPK: regulating energy balance at the cellular and whole body levels,” Physiology Journal, vol. 29, no. 2, pp. 99–107, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Racioppi and A. R. Means, “Calcium/calmodulin-dependent protein kinase kinase 2: roles in signaling and pathophysiology,” The Journal of Biological Chemistry, vol. 287, no. 38, pp. 31658–31665, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. K. A. Coughlan, R. J. Valentine, N. B. Ruderman, and A. K. Saha, “AMPK activation: a therapeutic target for type 2 diabetes?” Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy, vol. 7, pp. 241–253, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. G. L. Russo, M. Russo, and P. Ungaro, “AMP-activated protein kinase: a target for old drugs against diabetes and cancer,” Biochemical Pharmacology, vol. 86, no. 3, pp. 339–350, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Paradies, V. Paradies, F. M. Ruggiero, and G. Petrosillo, “Oxidative stress, cardiolipin and mitochondrial dysfunction in nonalcoholic fatty liver disease,” World Journal of Gastroenterology, vol. 20, no. 39, pp. 14205–14218, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Koliaki and M. Roden, “Hepatic energy metabolism in human diabetes mellitus, obesity and non-alcoholic fatty liver disease,” Molecular and Cellular Endocrinology, vol. 379, no. 1-2, pp. 35–42, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Schönfeld and L. Wojtczak, “Fatty acids as modulators of the cellular production of reactive oxygen species,” Free Radical Biology & Medicine, vol. 45, no. 3, pp. 231–241, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Garcia-Ruiz, A. Colell, A. Morales, N. Kaplowitz, and J. C. Fernandez-Checa, “Role of oxidative stress generated from the mitochondrial electron transport chain and mitochondrial glutathione status in loss of mitochondrial function and activation of transcription factor nuclear factor-κB: studies with isolated mitochondria and rat hepatocytes,” Molecular Pharmacology, vol. 48, no. 5, pp. 825–834, 1995. View at Google Scholar · View at Scopus
  35. K. Hensley, Y. Kotake, H. Sang et al., “Dietary choline restriction causes complex I dysfunction and increased H2O2 generation in liver mitochondria,” Carcinogenesis, vol. 21, no. 5, pp. 983–989, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Pessayre, “Role of mitochondria in non-alcoholic fatty liver disease,” Journal of Gastroenterology and Hepatology, vol. 22, supplement 1, pp. S20–S27, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. J. A. Sánchez-Alcázar, E. Schneider, M. A. Martínez et al., “Tumor necrosis factor-α increases the steady-state reduction of cytochrome b of the mitochondrial respiratory chain in metabolically inhibited L929 cells,” The Journal of Biological Chemistry, vol. 275, no. 18, pp. 13353–13361, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Higuchi, R. J. Proske, and E. T. H. Yeh, “Inhibition of mitochondrial respiratory chain complex I by TNF results in cytochrome c release, membrane permeability transition, and apoptosis,” Oncogene, vol. 17, no. 19, pp. 2515–2524, 1998. View at Publisher · View at Google Scholar · View at Scopus