Cytotoxic effect of evodiamine in SGC-7901 human gastric adenocarcinoma cells via simultaneous induction of apoptosis and autophagy

Oncology Reports

Volumn 27, Issue 5, 2012, Pages 1481-1487

  Rasul, Azhar ^a   Yu, Bo ^b   Zhong, Lili ^a   Khan, Muhammad ^a   Yang, Hong ^b   Ma, Tonghui ^a,b  

^a JILIN UNIVERSITY   (China)

^b LIAONING NORMAL UNIVERSITY   (China)

Author keywords

Apoptosis; Evodiamine; G2 M phase arrest; Natural compounds; SGC 7901 cells

Indexed keywords

3 METHYLADENINE; BECLIN 1; EVODIAMINE; PROTEIN BAX; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; AUTOPHAGY; CARCINOMA CELL; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL PROLIFERATION; CELL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH ADENOCARCINOMA; UPREGULATION;

ADENOCARCINOMA; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BCL-2-ASSOCIATED X PROTEIN; CELL CYCLE; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE PROTEINS; PLANT EXTRACTS; PROTO-ONCOGENE PROTEINS C-BCL-2; QUINAZOLINES; STOMACH NEOPLASMS;

EID: 84863252809     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2012.1694     Document Type: Article

References (52)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127: 2893-2917, 2010.
2. Yang L, Parkin DM, Ferlay J, Li L and Chen Y: Estimates of cancer incidence in China for 2000 and projections for 2005. Cancer Epidemiol Biomarkers Prev 14: 243-250, 2005. (Pubitemid 40165308)
3. Amin AR, Kucuk O, Khuri FR and Shin DM: Perspectives for cancer prevention with natural compounds. J Clin Oncol 27: 2712-2725, 2009.
4. Cragg GM and Newman DJ: Plants as a source of anti-cancer agents. J Ethnopharmacol 100: 72-79, 2005. (Pubitemid 41073525)
5. Lee TJ, Kim EJ, Kim S, et al: Caspase-dependent and caspase-independent apoptosis induced by evodiamine in human leukemic U937 cells. Mol Cancer Ther 5: 2398-2407, 2006. (Pubitemid 44530477)
6. Wang C, Wang MW, Tashiro S, Onodera S and Ikejima T: Evodiamine induced human melanoma A375-S2 cell death partially through interleukin 1 mediated pathway. Biol Pharm Bull 28: 984-989, 2005. (Pubitemid 40880301)
7. Yu X, Wu DZ, Yuan JY, Zhang RR and Hu ZB: Gastroprotective effect of fructus evodiae water extract on ethanol-induced gastric lesions in rats. Am J Chin Med 34: 1027-1035, 2006. (Pubitemid 44921247)
8. Liao CH, Pan SL, Guh JH, et al: Antitumor mechanism of evodiamine, a constituent from Chinese herb Evodiae fructus, in human multiple-drug resistant breast cancer NCI/ADR-RES cells in vitro and in vivo. Carcinogenesis 26: 968-975, 2005. (Pubitemid 41214326)
9. Chen MC, Yu CH, Wang SW, et al: Anti-proliferative effects of evodiamine on human thyroid cancer cell line ARO. J Cell Biochem 110: 1495-1503, 2010.
10. Wang XN, Han X, Xu LN, et al: Enhancement of apoptosis of human hepatocellular carcinoma SMMC-7721 cells through synergy of berberine and evodiamine. Phytomedicine 15: 1062-1068, 2008.
11. Huang DM, Guh JH, Huang YT, Chueh SC, Chiang PC and Teng CM: Induction of mitotic arrest and apoptosis in human prostate cancer pc-3 cells by evodiamine. J Urol 173: 256-261, 2005.
12. Kan SF, Huang WJ, Lin LC and Wang PS: Inhibitory effects of evodiamine on the growth of human prostate cancer cell line LNCaP. Int J Cancer 110: 641-651, 2004. (Pubitemid 38746021)
13. Kan SF, Yu CH, Pu HF, Hsu JM, Chen MJ and Wang PS: Anti-proliferative effects of evodiamine on human prostate cancer cell lines DU145 and PC3. J Cell Biochem 101: 44-56, 2007. (Pubitemid 46652571)
14. Sun HL, Liu YN, Huang YT, et al: YC-1 inhibits HIF-1 expression in prostate cancer cells: contribution of Akt/NF-κB signaling to HIF-1α accumulation during hypoxia. Oncogene 26: 3941-3951, 2007.
15. Huang YC, Guh JH and Teng CM: Induction of mitotic arrest and apoptosis by evodiamine in human leukemic T-lymphocytes. Life Sci 75: 35-49, 2004.
16. Wang C, Li S and Wang MW: Evodiamine-induced human melanoma A375-S2 cell death was mediated by PI3K/Akt/caspase and Fas-L/NF-kappaB signaling pathways and augmented by ubiquitin-proteasome inhibition. Toxicol In Vitro 24: 898-904, 2010.
17. Yang J, Wu LJ, Tashino S, Onodera S and Ikejima T: Critical roles of reactive oxygen species in mitochondrial permeability transition in mediating evodiamine-induced human melanoma A375-S2 cell apoptosis. Free Radic Res 41: 1099-1108, 2007. (Pubitemid 47470847)
18. Yang J, Wu LJ, Tashiro S, Onodera S and Ikejima T: Nitric oxide activated by p38 and NF-κB facilitates apoptosis and cell cycle arrest under oxidative stress in evodiamine-treated human melanoma A375-S2 cells. Free Radic Res 42: 1-11, 2008. (Pubitemid 351372186)
19. Fei XF, Wang BX, Li TJ, et al: Evodiamine, a constituent of Evodiae fructus, induces anti-proliferating effects in tumor cells. Cancer Sci 94: 92-98, 2003. (Pubitemid 36575865)
20. Yang J, Wu LJ, Tashino S, Onodera S and Ikejima T: Reactive oxygen species and nitric oxide regulate mitochondria-dependent apoptosis and autophagy in evodiamine-treated human cervix carcinoma HeLa cells. Free Radic Res 42: 492-504, 2008. (Pubitemid 351935163)
21. Ogasawara M, Matsubara T and Suzuki H: Screening of natural compounds for inhibitory activity on colon cancer cell migration. Biol Pharm Bull 24: 720-723, 2001. (Pubitemid 32586670)
22. Ogasawara M, Matsubara T and Suzuki H: Inhibitory effects of evodiamine on in vitro invasion and experimental lung metastasis of murine colon cancer cells. Biol Pharm Bull 24: 917-920, 2001. (Pubitemid 32750318)
23. Xu ML, Li G, Moon DC, et al: Cytotoxicity and DNA topoisomerase inhibitory activity of constituents isolated from the fruits of Evodia officinalis. Arch Pharm Res 29: 541-547, 2006. (Pubitemid 44199353)
24. Zhang C, Fan X, Xu X, Yang X, Wang X and Liang HP: Evodiamine induces caspase-dependent apoptosis and S phase arrest in human colon lovo cells. Anticancer Drugs 21: 766-776, 2010.
25. Yang ZG, Chen AQ and Liu B: Antiproliferation and apoptosis induced by evodiamine in human colorectal carcinoma cells (COLO-205). Chem Biodivers 6: 924-933, 2009.
26. Ogasawara M, Matsunaga T, Takahashi S, Saiki I and Suzuki H: Anti-invasive and metastatic activities of evodiamine. Biol Pharm Bull 25: 1491-1493, 2002. (Pubitemid 39663174)
27. Bursch W: The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ 8: 569-581, 2001.
28. Leist M and Jaattela M: Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2: 589-598, 2001. (Pubitemid 33674010)
29. Galluzzi L, Maiuri MC, Vitale I, et al: Cell death modalities: classification and pathophysiological implications. Cell Death Differ 14: 1237-1243, 2007. (Pubitemid 46969863)
30. Klionsky DJ and Emr SD: Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721, 2000. (Pubitemid 32004796)
31. Yoshimori T: Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Commun 313: 453-458, 2004.
32. Wang H, Haridas V, Gutterman JU and Xu ZX: Natural triterpenoid avicins selectively induce tumor cell death. Commun Integr Biol 3: 205-208, 2010.
33. Aoki H, Takada Y, Kondo S, Sawaya R, Aggarwal BB and Kondo Y: Evidence that curcumin suppresses the growth of malignant gliomas in vitro and in vivo through induction of autophagy: role of Akt and extracellular signal-regulated kinase signaling pathways. Mol Pharmacol 72: 29-39, 2007. (Pubitemid 46998522)
34. Xu ZX, Liang J, Haridas V, et al: A plant triterpenoid, avicin D, induces autophagy by activation of AMP-activated protein kinase. Cell Death Differ 14: 1948-1957, 2007. (Pubitemid 350011670)
35. Scherz-Shouval R and Elazar Z: ROS, mitochondria and the regulation of autophagy. Trends Cell Biol 17: 422-427, 2007. (Pubitemid 47499043)
36. Rasul A, Khan M, Yu B, Ma T and Yang H: Xanthoxyletin, a coumarin induces S phase arrest and apoptosis in human gastric adenocarcinoma SGC-7901 cells. Asian Pac J Cancer Prev 12: 1219-1223, 2011.
37. Yu J, Guo QL, You QD, et al: Gambogic acid-induced G2/M phase cell-cycle arrest via disturbing CDK7-mediated phosphorylation of CDC2/p34 in human gastric carcinoma BGC-823 cells. Carcinogenesis 28: 632-638, 2007. (Pubitemid 46523358)
38. Kanzawa T, Kondo Y, Ito H, Kondo S and Germano I: Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res 63: 2103-2108, 2003. (Pubitemid 36538613)
39. Levine B and Yuan J: Autophagy in cell death: an innocent convict? J Clin Invest 115: 2679-2688, 2005. (Pubitemid 41434392)
40. Kanzawa T, Zhang L, Xiao L, Germano IM, Kondo Y and Kondo S: Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene 24: 980-991, 2005. (Pubitemid 40313875)
41. Li DD, Guo JF, Huang JJ, et al: Rhabdastrellic acid-A induced autophagy-associated cell death through blocking Akt pathway in human cancer cells. PLoS One 5: e12176, 2010.
42. Daido S, Kanzawa T, Yamamoto A, Takeuchi H, Kondo Y and Kondo S: Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res 64: 4286-4293, 2004. (Pubitemid 38802435)
43. Paglin S, Hollister T, Delohery T, et al: A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 61: 439-444, 2001. (Pubitemid 32128593)
44. Liang XH, Jackson S, Seaman M, et al: Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402: 672-676, 1999. (Pubitemid 129516338)
45. Burlacu A: Regulation of apoptosis by Bcl-2 family proteins. J Cell Mol Med 7: 249-257, 2003.
46. Danial NN: BCL-2 family proteins: critical checkpoints of apoptotic cell death. Clin Cancer Res 13: 7254-7263, 2007.
47. Grana X and Reddy EP: Cell cycle control in mammalian cells: role of cyclins, cyclin dependent kinases (CDKs), growth suppressor genes and cyclin-dependent kinase inhibitors (CKIs). Oncogene 11: 211-219, 1995.
48. Kastan MB, Canman CE and Leonard CJ: P53, cell cycle control and apoptosis: implications for cancer. Cancer Metastasis Rev 14: 3-15, 1995.
49. Pavletich NP: Mechanisms of cyclin-dependent kinase regulation: structures of Cdks, their cyclin activators, and Cip and INK4 inhibitors. J Mol Biol 287: 821-828, 1999.
50. Jiang J and Hu C: Evodiamine: a novel anti-cancer alkaloid from Evodia rutaecarpa. Molecules 14: 1852-1859, 2009.
51. Mantena SK, Sharma SD and Katiyar SK: Berberine, a natural product, induces G1-phase cell cycle arrest and caspase-3-dependent apoptosis in human prostate carcinoma cells. Mol Cancer Ther 5: 296-308, 2006.
52. Srivastava JK and Gupta S: Tocotrienol-rich fraction of palm oil induces cell cycle arrest and apoptosis selectively in human prostate cancer cells. Biochem Biophys Res Commun 346: 447-453, 2006. (Pubitemid 43902706)