Blocking autophagic flux enhances matrine-induced apoptosis in human hepatoma cells

International Journal of Molecular Sciences

Volumn 14, Issue 12, 2013, Pages 23212-23230

  Wang, Li ^a   Gao, Chun ^b   Yao, Shukun ^a,b   Xie, Bushan ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b CHINA JAPAN FRIENDSHIP HOSPITAL   (China)

Author keywords

Apoptosis; Autophagic inhibitor; Autophagy; Chloroquine; Hepatocellular carcinoma; Matrine

Indexed keywords

BECLIN 1; CASPASE 3; CASPASE 8; CASPASE 9; CHLOROQUINE; MAMMALIAN TARGET OF RAPAMYCIN; MATRINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; ALKALOID; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, HUMAN; CASPASE; LIGHT CHAIN 3, HUMAN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MTOR PROTEIN, HUMAN; P62 PROTEIN, HUMAN; QUINOLIZINE DERIVATIVE; RNA BINDING PROTEIN; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; AUTOPHAGIC FLUX; AUTOPHAGY; CANCER CELL CULTURE; CELL ACTIVITY; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; COLONY FORMATION; COLONY FORMING CELL; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME INDUCTION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO GENE TRANSFER; LIVER CELL CARCINOMA; PLASMID; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; HEPG2 CELL LINE; LIVER TUMOR; METABOLISM; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOXICITY; TUMOR CELL LINE; UPREGULATION;

ALKALOIDS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CARCINOMA, HEPATOCELLULAR; CASPASES; CELL LINE, TUMOR; CHLOROQUINE; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; QUINOLIZINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UP-REGULATION;

EID: 84888364365     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141223212     Document Type: Article

References (41)

1. Chen, W. Q.; Zheng, R. S.; Zhang, S. W. Liver cancer incidence and mortality in China, 2009. Chin. J. Cancer 2013, 32, 162-169.
2. Llovet, J. M.; Bruix, J. Systematic review of randomized trials for unresectable hepatocellular carcinoma: Chemoembolization improves survival. Hepatology 2003, 37, 429-442.
3. El-Serag, H. B.; Siegel, A. B.; Davila, J. A.; Shaib, Y. H.; Cayton-Woody, M.; McBride, R.; McGlynn, K. A. Treatment and outcomes of treating of hepatocellular carcinoma among medicare recipients in the United States: A population-based study. J. Hepatol. 2006, 44, 158-166.
4. Samuel, M.; Chow, P. K.; Chan, S. E.; Machin, D.; Soo, K. C. Neoadjuvant and adjuvant therapy for surgical resection of hepatocellular carcinoma. Cochrane Database Syst. Rev. 2009, doi: 10. 1002/14651858. CD001199. pub2.
5. Davila, J. A.; Duan, Z.; McGlynn, K. A.; El-Serag, H. B. Utilization and outcomes of palliative therapy for hepatocellular carcinoma: A population-based study in the United States. J. Clin. Gastroenterol. 2012, 46, 71-77.
6. Thomas, M. B.; O'Beirne, J. P.; Furuse, J.; Chan, A. T.; Abou-Alfa, G.; Johnson, P. Systemic therapy for hepatocellular carcinoma: Cytotoxic chemotherapy, targeted therapy and immunotherapy. Ann. Surg. Oncol. 2008, 15, 1008-1014.
7. Ang, C.; O'Reilly, E. M.; Abou-Alfa, G. K. Targeted agents and systemic therapy in hepatocellular carcinoma. Recent Results Cancer Res. 2013, 190, 225-246.
8. Zhang, J. P.; Zhang, M.; Zhou, J. P.; Liu, F. T.; Zhou, B.; Xie, W. F.; Guo, C. Antifibrotic effects of matrine on in vitro and in vivo models of liver fibrosis in rats. Acta Pharmacol. Sin. 2001, 22, 183-186.
9. Zhang, S.; Zhang, Y.; Zhuang, Y.; Wang, J.; Ye, J.; Zhang, S.; Wu, J.; Yu, K.; Han, Y. Matrine induces apoptosis in human acute myeloid leukemia cells via the mitochondrial pathway and Akt inactivation. PLoS One 2012, 7, e46853.
10. Li, Y.; Zhang, J.; Ma, H.; Chen, X.; Liu, T.; Jiao, Z.; He, W.; Wang, F.; Liu, X.; Zeng, X. Protective role of autophagy in matrineinduced gastric cancer cell death. Int. J. Oncol. 2013, 42, 1417-1426.
11. Ma, L.; Wen, S.; Zhan, Y.; He, Y.; Liu, X.; Jiang, J. Anticancer effects of the Chinese medicine matrine on murine hepatocellular carcinoma cells. Planta Med. 2008, 74, 245-251.
12. Qin, X. G.; Hua, Z.; Shuang, W.; Wang, Y. H.; Cui, Y. D. Effects of matrine on HepG2 cell proliferation and expression of tumor relevant proteins in vitro. Pharm. Biol. 2010, 48, 275-281.
13. Liu, T.; Song, Y.; Chen, H.; Pan, S.; Sun, X. Matrine inhibits proliferation and induces apoptosis of pancreatic cancer cells in vitro and in vivo. Biol. Pharm. Bull. 2010, 33, 1740-1745.
14. Zhang, J. Q.; Li, Y. M.; Liu, T.; He, W. T.; Chen, Y. T.; Chen, X. H.; Li, X.; Zhou, W. C.; Yi, J. F.; Ren, Z. J. Antitumor effect of matrine in human hepatoma G2 cells by inducing apoptosis and autophagy. World J. Gastroenterol. 2010, 16, 4281-4290.
15. Levine, B.; Kroemer, G. Autophagy in the pathogenesis of disease. Cell 2008, 132, 27-42.
16. Chen, S.; Rehman, S. K.; Zhang, W.; Wen, A.; Yao, L.; Zhang, J. Autophagy is a therapeutic target in anticancer drug resistance. Biochim. Biophys. Acta 2010, 1806, 220-229.
17. Janku, F.; McConkey, D. J.; Hong, D. S.; Kurzrock, R. Autophagy as a target for anticancer therapy. Nat. Rev. Clin. Oncol. 2011, 8, 528-539.
18. Zhang, X. J.; Chen, S.; Huang, K. X.; Le, W. D. Why should autophagic flux be assessed? Acta Pharmacol. Sin. 2013, 34, 595-599.
19. Fan, C.; Wang, W.; Zhao, B.; Zhang, S.; Miao, J. Chloroquine inhibits cell growth and induces cell death in A549 lung cancer cells. Bioorg. Med. Chem. 2006, 14, 3218-3222.
20. Kabeya, Y.; Mizushima, N.; Ueno, T.; Yamamoto, A.; Kirisako, T.; Noda, T.; Kominami, E.; Ohsumi, Y.; Yoshimori, T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19, 5720-5728.
21. Komatsu, M.; Waguri, S.; Koike, M.; Sou, Y. S.; Ueno, T.; Hara, T.; Mizushima, N.; Iwata, J.; Ezaki, J.; Murata, S.; et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007, 131, 1149-1163.
22. Amaravadi, R. K.; Thompson, C. B. The roles of therapy-induced autophagy and necrosis in cancer treatment. Clin. Cancer Res. 2007, 13, 7271-7279.
23. Wirawan, E.; Lippens, S.; Vanden, B. T.; Romagnoli, A.; Fimia, G. M.; Piacentini, M.; Vandenabeele, P. Beclin-1: A role in membrane dynamics and beyond. Autophagy 2012, 8, 6-17.
24. Kruidering, M.; Evan, G. I. Caspase-8 in apoptosis: The beginning of "the end"? IUBMB Life 2000, 50, 85-90.
25. Porter, A. G.; Janicke, R. U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999, 6, 99-104.
26. Shi, Y. H.; Ding, Z. B.; Zhou, J.; Hui, B.; Shi, G. M.; Ke, A. W.; Wang, X. Y.; Dai, Z.; Peng, Y. F.; Gu, C. Y.; et al. Targeting autophagy enhances sorafenib lethality for hepatocellular carcinoma via ER stress-related apoptosis. Autophagy 2011, 7, 1159-1172.
27. Xie, B. S.; Zhao, H. C.; Yao, S. K.; Zhuo, D. X.; Jin, B.; Lv, D. C.; Wu, C. L.; Ma, D. L.; Gao, C.; Shu, X. M.; et al. Autophagy inhibition enhances etoposide-induced cell death in human hepatoma G2 cells. Int. J. Mol. Med. 2011, 27, 599-606.
28. Wu, J.; Hu, D.; Zhang, R. Depletion of Bmi-1 enhances 5-fluorouracil-induced apoptosis and autophagy in hepatocellular carcinoma cells. Oncol. Lett. 2012, 4, 723-726.
29. Klionsky, D. J.; Abdalla, F. C.; Abeliovich, H.; Abraham, R. T.; Acevedo-Arozena, A.; Adeli, K.; Agholme, L.; Agnello, M.; Agostinis, P.; Aguirre-Ghiso, J. A.; et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8, 445-544.
30. Shingu, T.; Fujiwara, K.; Bogler, O.; Akiyama, Y.; Moritake, K.; Shinojima, N.; Tamada, Y.; Yokoyama, T.; Kondo, S. Stage-specific effect of inhibition of autophagy on chemotherapy-induced cytotoxicity. Autophagy 2009, 5, 537-539.
31. Amaravadi, R. K.; Lippincott-Schwartz, J.; Yin, X. M.; Weiss, W. A.; Takebe, N.; Timmer, W.; di Paola, R. S.; Lotze, M. T.; White, E. Principles and current strategies for targeting autophagy for cancer treatment. Clin. Cancer Res. 2011, 17, 654-666.
32. Gao, L.; Song, J. R.; Zhang, J. W.; Zhao, X.; Zhao, Q. D.; Sun, K.; Deng, W. J.; Li, R.; Lv, G.; Cheng, H. Y.; et al. Chloroquine promotes the anticancer effect of TACE in a rabbit VX2 liver tumor model. Int. J. Biol. Sci. 2013, 9, 322-330.
33. Cui, J.; Gong, Z.; Shen, H. M. The role of autophagy in liver cancer: Molecular mechanisms and potential therapeutic targets. Biochim. Biophys. Acta 2013, 1836, 15-26.
34. Kang, R.; Zeh, H. J.; Lotze, M. T.; Tang, D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011, 18, 571-580.
35. Zhou, L.; Huang, Y.; Li, J.; Wang, Z. The mTOR pathway is associated with the poor prognosis of human hepatocellular carcinoma. Med. Oncol. 2010, 27, 255-261.
36. Villanueva, A.; Chiang, D. Y.; Newell, P.; Peix, J.; Thung, S.; Alsinet, C.; Tovar, V.; Roayaie, S.; Minguez, B.; Sole, M.; et al. Pivotal role of mTOR signaling in hepatocellular carcinoma. Gastroenterology 2008, 135, doi: 10. 1053/j. gastro. 2008. 08. 008.
37. Zhou, Q.; Lui, V. W.; Yeo, W. Targeting the PI3K/Akt/mTOR pathway in hepatocellular carcinoma. Future Oncol. 2011, 7, 1149-1167.
38. Li, L. Q.; Li, X. L.; Wang, L.; Du, W. J.; Guo, R.; Liang, H. H.; Liu, X.; Liang, D. S.; Lu, Y. J.; Shan, H. L.; et al. Matrine inhibits breast cancer growth via miR-21/PTEN/Akt pathway in MCF-7 cells. Cell Physiol. Biochem. 2012, 30, 631-641.
39. Lamoureux, F.; Zoubeidi, A. Dual inhibition of autophagy and the AKT pathway in prostate cancer. Autophagy 2013, 9, 1119-1120.
40. Li, J. R.; Cheng, C. L.; Yang, C. R.; Ou, Y. C.; Wu, M. J.; Ko, J. L. Dual inhibitor of phosphoinositide 3-kinase/mammalian target of rapamycin NVP-BEZ235 effectively inhibits cisplatin-resistant urothelial cancer cell growth through autophagic flux. Toxicol. Lett. 2013, 220, 267-276.
41. Chang, Z.; Shi, G.; Jin, J.; Guo, H.; Guo, X.; Luo, F.; Song, Y.; Jia, X. Dual PI3K/mTOR inhibitor NVP-BEZ235-induced apoptosis of hepatocellular carcinoma cell lines is enhanced by inhibitors of autophagy. Int. J. Mol. Med. 2013, 31, 1449-1456.