Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 732516, 13 pages
http://dx.doi.org/10.1155/2014/732516
Research Article

Baicalein Induces Apoptosis and Autophagy via Endoplasmic Reticulum Stress in Hepatocellular Carcinoma Cells

1Department of Hepatobiliary Surgery, the Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing, Jiangsu 210008, China
2Department of Hepatobiliary Surgery, Nanjing Drum Tower Hospital Clinical College of Traditional Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu 210008, China
3Department of Hepatobiliary Surgery, Nanjing Drum Tower Hospital Clinical College of Nanjing Medical University, Nanjing, Jiangsu 210008, China
4School of Medicine, Nanjing University, Nanjing, Jiangsu 210093, China
5The Comprehensive Cancer Center, the Affiliated Drum Tower Hospital of Nanjing University Medical School, Nanjing, Jiangsu 210008, China
6The Comprehensive Cancer Center, Nanjing Drum Tower Hospital Clinical College of Traditional Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing, Jiangsu 210008, China

Received 27 March 2014; Accepted 5 May 2014; Published 3 June 2014

Academic Editor: Jingmin Zhao

Copyright © 2014 Zhongxia Wang 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. A. Jemal, F. Bray, M. M. Center, J. Ferlay, E. Ward, and D. Forman, “Global cancer statistics,” CA: Cancer Journal for Clinicians, vol. 61, no. 2, pp. 69–90, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. H. B. El-Serag, “Hepatocellular carcinoma,” The New England Journal of Medicine, vol. 365, no. 12, pp. 1118–1127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. J. M. Luk, X. Wang, P. Liu et al., “Traditional Chinese herbal medicines for treatment of liver fibrosis and cancer: from laboratory discovery to clinical evaluation,” Liver International, vol. 27, no. 7, pp. 879–890, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Forner, J. M. Llovet, and J. Bruix, “Hepatocellular carcinoma,” The Lancet, vol. 379, no. 9822, pp. 1245–1255, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. G. Ramakrishna, A. Rastogi, N. Trehanpati et al., “From cirrhosis to hepatocellular carcinoma: new molecular insights on inflammation and cellular senescence,” Liver Cancer, vol. 2, pp. 367–383, 2013. View at Publisher · View at Google Scholar
  6. L. Dara, C. Ji, and N. Kaplowitz, “The contribution of endoplasmic reticulum stress to liver diseases,” Hepatology, vol. 53, no. 5, pp. 1752–1763, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Malhi and R. J. Kaufman, “Endoplasmic reticulum stress in liver disease,” Journal of Hepatology, vol. 54, no. 4, pp. 795–809, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Xu, B. Bailly-Maitre, and J. C. Reed, “Endoplasmic reticulum stress: cell life and death decisions,” Journal of Clinical Investigation, vol. 115, no. 10, pp. 2656–2664, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Su, L. Zhou, X. Kong et al., “Endoplasmic reticulum is at the crossroads of autophagy, inflammation, and apoptosis signaling pathways and participates in the pathogenesis of diabetes mellitus,” Journal of Diabetes Research, vol. 2013, Article ID 193461, 6 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Moretti, Y. I. Cha, K. J. Niermann, and B. Lu, “Switch between apoptosis and autophagy: radiation-induced endoplasmic reticulum stress?” Cell Cycle, vol. 6, no. 7, pp. 793–798, 2007. View at Google Scholar · View at Scopus
  11. M. Moenner, O. Pluquet, M. Bouchecareilh, and E. Chevet, “Integrated endoplasmic reticulum stress responses in cancer,” Cancer Research, vol. 67, no. 22, pp. 10631–10634, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Shuda, N. Kondoh, N. Imazeki et al., “Activation of the ATF6, XBP1 and grp78 genes in human hepatocellular carcinoma: a possible involvement of the ER stress pathway in hepatocarcinogenesis,” Journal of Hepatology, vol. 38, no. 5, pp. 605–614, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. I. Kim, W. Xu, and J. C. Reed, “Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities,” Nature Reviews Drug Discovery, vol. 7, no. 12, pp. 1013–1030, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Moeini, H. Cornella, and A. Villanueva, “Emerging signaling pathways in hepatocellular carcinoma,” Liver Cancer, vol. 1, pp. 83–93, 2012. View at Publisher · View at Google Scholar
  15. P. di Fazio, M. Ocker, and R. Montalbano, “New drugs, old fashioned ways: ER stress induced cell death,” Current Pharmaceutical Biotechnology, vol. 13, no. 11, pp. 2228–2234, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. W.-H. Chang, C.-H. Chen, and F.-J. Lu, “Different effects of baicalein, baicalin and wogonin on mitochondrial function, glutathione content and cell cycle progression in human hepatoma cell lines,” Planta Medica, vol. 68, no. 2, pp. 128–132, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. W.-H. Chang, C.-H. Chen, R.-J. Gau et al., “Effect of baicalein on apoptosis of the human Hep G2 cell line was induced by mitochondrial dysfunction,” Planta Medica, vol. 68, no. 4, pp. 302–306, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. Y.-H. Zheng, L.-H. Yin, T. H. M. Grahn, A.-F. Ye, Y.-R. Zhao, and Q.-Y. Zhang, “Anticancer effects of baicalein on hepatocellular carcinoma cells,” Phytotherapy Research, 2014. View at Publisher · View at Google Scholar
  19. X.-M. Xu, G.-J. Yuan, J.-J. Deng et al., “Inhibition of 12-lipoxygenase reduces proliferation and induces apoptosis of hepatocellular carcinoma cells in vitro and in vivo,” Hepatobiliary and Pancreatic Diseases International, vol. 11, no. 2, pp. 193–202, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Xu, N. Lu, H. Zhang et al., “Wogonin induced cytotoxicity in human hepatocellular carcinoma cells by activation of unfolded protein response and inactivation of AKT,” Hepatology Research, vol. 43, no. 8, pp. 890–905, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. C. C. Chou, S. L. Pan, C. M. Teng, and J. H. Guh, “Pharmacological evaluation of several major ingredients of Chinese herbal medicines in human hepatoma Hep3B cells,” European Journal of Pharmaceutical Sciences, vol. 19, no. 5, pp. 403–412, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Chen, S. Zhang, Y. Ji et al., “Baicalein inhibits the invasion and metastatic capabilities of hepatocellular carcinoma cells via down-regulation of the ERK pathway,” PLoS ONE, vol. 8, no. 9, Article ID e72927, 2013. View at Publisher · View at Google Scholar
  23. R.-R. Liang, S. Zhang, J.-A. N. Qi et al., “Preferential inhibition of hepatocellular carcinoma by the flavonoid Baicalein through blocking MEK-ERK signaling,” International Journal of Oncology, vol. 41, no. 3, pp. 969–978, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. Y.-W. Chiu, T.-H. Lin, W.-S. Huang et al., “Baicalein inhibits the migration and invasive properties of human hepatoma cells,” Toxicology and Applied Pharmacology, vol. 255, no. 3, pp. 316–326, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. Y.-H. Shi, Z.-B. Ding, J. Zhou et al., “Targeting autophagy enhances sorafenib lethality for hepatocellular carcinoma via ER stress-related apoptosis,” Autophagy, vol. 7, no. 10, pp. 1159–1172, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. W.-X. Ding, H.-M. Ni, W. Gao et al., “Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival,” Journal of Biological Chemistry, vol. 282, no. 7, pp. 4702–4710, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. Z. Wang, Y. Cao, C. Jiang, G. Yang, J. Wu, and Y. Ding, “Lack of association of two common polymorphisms rs2910164 and rs11614913 with susceptibility to hepatocellular carcinoma: a meta-analysis,” PLoS ONE, vol. 7, no. 6, Article ID e40039, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. J. M. Llovet, M. Schwartz, and V. Mazzaferro, “Resection and liver transplantation for hepatocellular carcinoma,” Seminars in Liver Disease, vol. 25, no. 2, pp. 181–200, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. C. Shen, Z. Z. Lin, C. H. Hsu et al., “Clinical trials in hepatocellular carcinoma: an update,” Liver Cancer, vol. 2, pp. 345–364, 2013. View at Publisher · View at Google Scholar
  30. J. Shindoh, A. Kaseb, and J. N. Vauthey, “Surgical strategy for liver cancers in the era of effective chemotherapy,” Liver Cancer, vol. 2, pp. 47–54, 2013. View at Publisher · View at Google Scholar
  31. V. di Marco, F. de Vita, J. Koskinas, D. Semela, P. Toniutto, and C. Verslype, “Sorafenib: from literature to clinical practice,” Annals of Oncology, vol. 24, supplement 2, pp. ii30–ii37, 2013. View at Google Scholar · View at Scopus
  32. G. Zhang, Z. Wang, W. Luo, H. Jiao, J. Wu, and C. Jiang, “Expression of potential cancer stem cell marker ABCG2 is associated with malignant behaviors of hepatocellular carcinoma,” Gastroenterology Research and Practice, vol. 2013, Article ID 782581, 12 pages, 2013. View at Publisher · View at Google Scholar
  33. Z. Wang, J. Wu, G. Zhang, Y. Cao, C. Jiang, and Y. Ding, “Associations of miR-499 and miR-34b/c polymorphisms with susceptibility to hepatocellular carcinoma: an evidence-based evaluation,” Gastroenterology Research and Practice, vol. 2013, Article ID 719202, 8 pages, 2013. View at Publisher · View at Google Scholar
  34. R. Finn, “Emerging targeted strategies in advanced hepatocellular carcinoma,” Seminars in Liver Disease, vol. 33, supplement 1, pp. S11–S19, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Gong, “Identifying the targets for treatment of liver fibrosis and hepatocellular carcinoma from both Western medicine and Chinese medicine,” Chinese Journal of Integrative Medicine, vol. 18, no. 4, pp. 245–249, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Chen and J. Zhu, “Anti-HBV effect of individual traditional Chinese herbal medicine in vitro and in vivo: an analytic review,” Journal of Viral Hepatitis, vol. 20, no. 7, pp. 445–452, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Okita, Q. Li, T. Murakamio, and M. Takahashi, “Anti-growth effects with components of Sho-saiko-to (TJ-9) on cultured human hepatoma cells,” European Journal of Cancer Prevention, vol. 2, no. 2, pp. 169–175, 1993. View at Google Scholar · View at Scopus
  38. Y. Motoo and N. Sawabu, “Antitumor effects of saikosaponins, baicalin and baicalein on human hepatoma cell lines,” Cancer Letters, vol. 86, no. 1, pp. 91–95, 1994. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Yu, F. Qu, Y. Mao et al., “Different extraction pretreatments significantly change the flavonoid contents of Scutellaria baicalensis,” Pharmaceutical Biology, vol. 51, no. 10, pp. 1228–1235, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Matsuzaki, N. Kurokawa, S. Terai, Y. Matsumura, N. Kobayashi, and K. Okita, “Cell death induced by baicalein in human hepatocellular carcinoma cell lines,” Japanese Journal of Cancer Research, vol. 87, no. 2, pp. 170–177, 1996. View at Google Scholar · View at Scopus
  41. H.-M. Kuo, H.-C. Tsai, Y.-L. Lin et al., “Mitochondrial-dependent caspase activation pathway is involved in baicalein-induced apoptosis in human hepatoma J5 cells,” International Journal of Oncology, vol. 35, no. 4, pp. 717–724, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Kimata and K. Kohno, “Endoplasmic reticulum stress-sensing mechanisms in yeast and mammalian cells,” Current Opinion in Cell Biology, vol. 23, no. 2, pp. 135–142, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. S. E. Logue, P. Cleary, S. Saveljeva, and A. Samali, “New directions in ER stress-induced cell death,” Apoptosis, vol. 18, no. 5, pp. 537–546, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. H. P. Harding, Y. Zhang, and D. Ron, “Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase,” Nature, vol. 397, pp. 271–274, 1999. View at Publisher · View at Google Scholar
  45. H. P. Harding, I. Novoa, Y. Zhang et al., “Regulated translation initiation controls stress-induced gene expression in mammalian cells,” Molecular Cell, vol. 6, no. 5, pp. 1099–1108, 2000. View at Google Scholar · View at Scopus
  46. X.-Z. Wang, H. P. Harding, Y. Zhang, E. M. Jolicoeur, M. Kuroda, and D. Ron, “Cloning of mammalian Ire1 reveals diversity in the ER stress responses,” EMBO Journal, vol. 17, no. 19, pp. 5708–5717, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. Y.-R. Chen, C. F. Meyer, and T.-H. Tan, “Persistent activation of c-Jun N-terminal kinase 1 (JNK1) in γ radiation-induced apoptosis,” Journal of Biological Chemistry, vol. 271, no. 2, pp. 631–634, 1996. View at Publisher · View at Google Scholar · View at Scopus
  48. F. J. Guo, Z. Xiong, X. Lu, M. Ye, X. Han, and R. Jiang, “ATF6 upregulates XBP1S and inhibits ER stress-mediated apoptosis in osteoarthritis cartilage,” Cellular Signalling, vol. 26, no. 2, pp. 332–342, 2014. View at Publisher · View at Google Scholar
  49. K. H. Tay, Q. Luan, A. Croft et al., “Sustained IRE1 and ATF6 signaling is important for survival of melanoma cells undergoing ER stress,” Cellular Signalling, vol. 26, pp. 287–294, 2014. View at Publisher · View at Google Scholar
  50. J. Groenendyk and M. Michalak, “Endoplasmic reticulum quality control and apoptosis,” Acta Biochimica Polonica, vol. 52, no. 2, pp. 381–395, 2005. View at Google Scholar · View at Scopus