Evodiamine induces apoptosis and enhances TRAIL-induced apoptosis in human bladder cancer cells through mTOR/S6K1-mediated downregulation of Mcl-1

International Journal of Molecular Sciences

Volumn 15, Issue 2, 2014, Pages 3154-3171

  Zhang, Tao ^a   Qu, Shanna ^b   Shi, Qi ^c   He, Dalin ^c   Jin, Xunbo ^a  

^a SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

^b SHANDONG UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

Bladder cancer; Evodiamine; Mcl 1; Mtor; S6k1; Trail

Indexed keywords

EVODIAMINE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN MCL 1; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; CFLAR PROTEIN, HUMAN; FLICE INHIBITORY PROTEIN; MCL1 PROTEIN, HUMAN; MESSENGER RNA; MTOR PROTEIN, HUMAN; MYELOID LEUKEMIA FACTOR 1; QUINAZOLINE DERIVATIVE; RIBOSOMAL PROTEIN S6 KINASE, 70KD, POLYPEPTIDE 1; S6 KINASE; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; BLADDER CANCER; CELL VIABILITY; CHEMOLUMINESCENCE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BLADDER TUMOR; CHEMISTRY; DRUG EFFECTS; EVODIA; GENETICS; METABOLISM; PATHOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CELL LINE, TUMOR; DOWN-REGULATION; EVODIA; HUMANS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; QUINAZOLINES; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TOR SERINE-THREONINE KINASES; URINARY BLADDER NEOPLASMS;

EID: 84894242800     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15023154     Document Type: Article

References (47)

1. Siegel, R.; Naishadham, D.; Jemal, A. Cancer statistics, 2012. CA Cancer J. Clin. 2012, 62, 10-29.
2. Babjuk, M.; Burger, M.; Zigeuner, R.; Shariat, S.F.; van Rhijn, B.W.; Comperat, E.; Sylvester, R.J.; Kaasinen, E.; Bohle, A.; Palou, R.J., et al. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: Update 2013. Eur. Urol. 2013, 64, 639-653.
3. Leopardo, D.; Cecere, S.C.; di Napoli, M.; Cavaliere, C.; Pisano, C.; Striano, S.; Marra, L.; Menna, L.; Claudio, L.; Perdona, S., et al. Intravesical chemo-immunotherapy in non muscle invasive bladder cancer. Eur. Rev. Med. Pharmacol. Sci. 2013, 17, 2145-2158.
4. Herr, H.W.; Morales, A. History of bacillus Calmette-Guerin and bladder cancer: An immunotherapy success story. J. Urol. 2008, 179, 53-56.
5. Shang, P.F.; Kwong, J.; Wang, Z.P.; Tian, J.; Jiang, L.; Yang, K.; Yue, Z.J.; Tian, J.Q. Intravesical Bacillus Calmette-Guerin versus epirubicin for Ta and T1 bladder cancer. Cochrane Database Syst. Rev. 2011, doi:10.1002/14651858.CD006885.pub2.
6. Schaefer, U.; Voloshanenko, O.; Willen, D.; Walczak, H. TRAIL: A multifunctional cytokine. Front. Biosci. 2007, 12, 3813-3824.
7. Herbst, R.S.; Eckhardt, S.G.; Kurzrock, R.; Ebbinghaus, S.; O'Dwyer, P.J.; Gordon, M.S.; Novotny, W.; Goldwasser, M.A.; Tohnya, T.M.; Lum, B.L., et al. Phase I dose-escalation study of recombinant human Apo2L/TRAIL, a dual proapoptotic receptor agonist, in patients with advanced cancer. J. Clin. Oncol. 2010, 28, 2839-2846.
8. Ludwig, A.T.; Moore, J.M.; Luo, Y.; Chen, X.; Saltsgaver, N.A.; O'Donnell, M.A.; Griffith, T.S. Tumor necrosis factor-related apoptosis-inducing ligand: A novel mechanism for Bacillus Calmette-Guerin-induced antitumor activity. Cancer Res. 2004, 64, 3386-3390.
9. Moibi, J.A.; Mak, A.L.; Sun, B.; Moore, R.B. Urothelial cancer cell response to combination therapy of gemcitabine and TRAIL. Int. J. Oncol. 2011, 39, 61-71.
10. Shimada, O.; Wu, X.; Jin, X.; Nouh, M.A.; Fiscella, M.; Albert, V.; Matsuda, T.; Kakehi, Y. Human agonistic antibody to tumor necrosis factor-related apoptosis-inducing ligand receptor 2 induces cytotoxicity and apoptosis in prostate cancer and bladder cancer cells. Urology 2007, 69, 395-401.
11. Zhang, L.; Fang, B. Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther. 2005, 12, 228-237.
12. Kauntz, H.; Bousserouel, S.; Gosse, F.; Raul, F. The flavonolignan silibinin potentiates TRAIL-induced apoptosis in human colon adenocarcinoma and in derived TRAIL-resistant metastatic cells. Apoptosis 2012, 17, 797-809.
13. Park, S.; Cho, D.H.; Andera, L.; Suh, N.; Kim, I. Curcumin enhances TRAIL-induced apoptosis of breast cancer cells by regulating apoptosis-related proteins. Mol. Cell. Biochem. 2013, 383, 39-48.
14. Yu, H.; Jin, H.; Gong, W.; Wang, Z.; Liang, H. Pharmacological actions of multi-target-directed evodiamine. Molecules 2013, 18, 1826-1843.
15. Wang, K.L.; Hsia, S.M.; Yeh, J.Y.; Cheng, S.C.; Wang, P.S.; Wang, S.W. Anti-Proliferative Effects of Evodiamine on Human Breast Cancer Cells. PLoS One 2013, 8, e67297.
16. Huang, D.M.; Guh, J.H.; Huang, Y.T.; Chueh, S.C.; Chiang, P.C.; Teng, C.M. Induction of mitotic arrest and apoptosis in human prostate cancer pc-3 cells by evodiamine. J. Urol. 2005, 173, 256-261.
17. Ogasawara, M.; Matsubara, T.; Suzuki, H. Inhibitory effects of evodiamine on in vitro invasion and experimental lung metastasis of murine colon cancer cells. Biol. Pharm. Bull. 2001, 24, 917-920.
18. Zhang, C.; Fan, X.; Xu, X.; Yang, X.; Wang, X.; Liang, H.P. Evodiamine induces caspase-dependent apoptosis and S phase arrest in human colon lovo cells. Anticancer Drugs 2010, 21, 766-776.
19. Wang, C.; Wang, M.W.; Tashiro, S.; Onodera, S.; Ikejima, T. Roles of SIRT1 and phosphoinositide 3-OH kinase/protein kinase C pathways in evodiamine-induced human melanoma A375-S2 cell death. J. Pharmacol. Sci. 2005, 97, 494-500.
20. Wang, C.; Li, S.; Wang, M.W. 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 2010, 24, 898-904.
21. Jiang, J.; Hu, C. Evodiamine: A novel anti-cancer alkaloid from Evodia rutaecarpa. Molecules 2009, 14, 1852-1859.
22. Wei, W.T.; Chen, H.; Wang, Z.H.; Ni, Z.L.; Liu, H.B.; Tong, H.F.; Guo, H.C.; Liu, D.L.; Lin, S.Z. Enhanced antitumor efficacy of gemcitabine by evodiamine on pancreatic cancer via regulating PI3K/Akt pathway. Int. J. Biol. Sci. 2012, 8, 1-14.
23. Liao, C.H.; Pan, S.L.; Guh, J.H.; Chang, Y.L.; Pai, H.C.; Lin, C.H.; Teng, C.M. 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 2005, 26, 968-975.
24. Steele, L.P.; Georgopoulos, N.T.; Southgate, J.; Selby, P.J.; Trejdosiewicz, L.K. Differential susceptibility to TRAIL of normal versus malignant human urothelial cells. Cell Death Differ. 2006, 13, 1564-1576.
25. White-Gilbertson, S.J.; Kasman, L.; McKillop, J.; Tirodkar, T.; Lu, P.; Voelkel-Johnson, C. Oxidative stress sensitizes bladder cancer cells to TRAIL mediated apoptosis by down-regulating anti-apoptotic proteins. J. Urol. 2009, 182, 1178-1185.
26. Abdulghani, J.; El-Deiry, W.S. TRAIL receptor signaling and therapeutics. Expert Opin. Ther. Targets 2010, 14, 1091-1108.
27. Kim, S.H.; Ricci, M.S.; El-Deiry, W.S. Mcl-1: A gateway to TRAIL sensitization. Cancer Res. 2008, 68, 2062-2064.
28. Wang, X.; Chen, W.; Zeng, W.; Bai, L.; Tesfaigzi, Y.; Belinsky, S.A.; Lin, Y. Akt-mediated eminent expression of c-FLIP and Mcl-1 confers acquired resistance to TRAIL-induced cytotoxicity to lung cancer cells. Mol. Cancer Ther. 2008, 7, 1156-1163.
29. Jacquemin, G.; Granci, V.; Gallouet, A.S.; Lalaoui, N.; Morle, A.; Iessi, E.; Morizot, A.; Garrido, C.; Guillaudeux, T.; Micheau, O. Quercetin-mediated Mcl-1 and survivin downregulation restores TRAIL-induced apoptosis in non-Hodgkin's lymphoma B cells. Haematologica 2012, 97, 38-46.
30. Maurer, U.; Charvet, C.; Wagman, A.S.; Dejardin, E.; Green, D.R. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol. Cell 2006, 21, 749-760.
31. Opferman, J.T. Unraveling MCL-1 degradation. Cell Death Differ. 2006, 13, 1260-1262.
32. Mills, J.R.; Hippo, Y.; Robert, F.; Chen, S.M.; Malina, A.; Lin, C.J.; Trojahn, U.; Wendel, H.G.; Charest, A.; Bronson, R.T., et al. mTORC1 promotes survival through translational control of Mcl-1. Proc. Natl. Acad. Sci. USA 2008, 105, 10853-10858.
33. Hong, S.E.; Kim, E.K.; Jin, H.O.; Kim, H.A.; Lee, J.K.; Koh, J.S.; Seol, H.; Kim, J.I.; Park, I.C.; Noh, W.C. S6K1 inhibition enhances tamoxifen-induced cell death in MCF-7 cells through translational inhibition of Mcl-1 and survivin. Cell Biol. Toxicol. 2013, 29, 273-282.
34. Viswanath, V.; Wu, Y.; Boonplueang, R.; Chen, S.; Stevenson, F.F.; Yantiri, F.; Yang, L.; Beal, M.F.; Andersen, J.K. Caspase-9 activation results in downstream caspase-8 activation and bid cleavage in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson's disease. J. Neurosci. 2001, 21, 9519-9528.
35. Ferreira, K.S.; Kreutz, C.; Macnelly, S.; Neubert, K.; Haber, A.; Bogyo, M.; Timmer, J.; Borner, C. Caspase-3 feeds back on caspase-8, Bid and XIAP in type I Fas signaling in primary mouse hepatocytes. Apoptosis 2012, 17, 503-515.
36. de Vries, J.F.; Wammes, L.J.; Jedema, I.; van Dreunen, L.; Nijmeijer, B.A.; Heemskerk, M.H.; Willemze, R.; Falkenburg, J.H.; Barge, R.M. Involvement of caspase-8 in chemotherapy-induced apoptosis of patient derived leukemia cell lines independent of the death receptor pathway and downstream from mitochondria. Apoptosis 2007, 12, 181-193.
37. Takada, Y.; Kobayashi, Y.; Aggarwal, B.B. Evodiamine abolishes constitutive and inducible NF-kappaB activation by inhibiting IkappaBalpha kinase activation, thereby suppressing NF-kappaB-regulated antiapoptotic and metastatic gene expression, up-regulating apoptosis, and inhibiting invasion. J. Biol. Chem. 2005, 280, 17203-17212.
38. Oka, N.; Tanimoto, S.; Taue, R.; Nakatsuji, H.; Kishimoto, T.; Izaki, H.; Fukumori, T.; Takahashi, M.; Nishitani, M.; Kanayama, H.O. Role of phosphatidylinositol-3 kinase/Akt pathway in bladder cancer cell apoptosis induced by tumor necrosis factor-related apoptosis-inducing ligand. Cancer Sci. 2006, 97, 1093-1098.
39. Ren, H.; Zhao, L.; Li, Y.; Yue, P.; Deng, X.; Owonikoko, T.K.; Chen, M.; Khuri, F.R.; Sun, S.Y. The PI3 kinase inhibitor NVP-BKM120 induces GSK3/FBXW7-dependent Mcl-1 degradation, contributing to induction of apoptosis and enhancement of TRAIL-induced apoptosis. Cancer Lett. 2013, 338, 229-238.
40. Murphy, A.C.; Weyhenmeyer, B.; Noonan, J.; Kilbride, S.M.; Schimansky, S.; Loh, K.P.; Kogel, D.; Letai, A.G.; Prehn, J.H.; Murphy, B.M. Modulation of Mcl-1 sensitizes glioblastoma to TRAIL-induced apoptosis. Apoptosis 2013, doi:10.1007/s10495-013-0935-2.
41. Clohessy, J.G.; Zhuang, J.; de Boer, J.; Gil-Gomez, G.; Brady, H.J. Mcl-1 interacts with truncated Bid and inhibits its induction of cytochrome c release and its role in receptor-mediated apoptosis. J. Biol. Chem. 2006, 281, 5750-5759.
42. Akgul, C. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell. Mol. Life Sci. 2009, 66, 1326-1336.
43. Liu, Y.N.; Pan, S.L.; Liao, C.H.; Huang, D.Y.; Guh, J.H.; Peng, C.Y.; Chang, Y.L.; Teng, C.M. Evodiamine represses hypoxia-induced inflammatory proteins expression and hypoxia-inducible factor 1alpha accumulation in RAW264.7. Shock 2009, 32, 263-269.
44. Guertin, D.A.; Sabatini, D.M. Defining the role of mTOR in cancer. Cancer Cell 2007, 12, 9-22.
45. Wei, G.; Twomey, D.; Lamb, J.; Schlis, K.; Agarwal, J.; Stam, R.W.; Opferman, J.T.; Sallan, S.E.; den Boer, M.L.; Pieters, R., et al. Gene expression-based chemical genomics identifies rapamycin as a modulator of MCL1 and glucocorticoid resistance. Cancer Cell 2006, 10, 331-342.
46. Choi, H.N.; Jin, H.O.; Kim, J.H.; Hong, S.E.; Kim, H.A.; Kim, E.K.; Lee, J.K.; Park, I.C.; Noh, W.C. Inhibition of S6K1 enhances glucose deprivation-induced cell death via downregulation of anti-apoptotic proteins in MCF-7 breast cancer cells. Biochem. Biophys. Res. Commun. 2013, 432, 123-128.
47. Zhao, L.; Yue, P.; Khuri, F.R.; Sun, S.Y. mTOR complex 2 is involved in regulation of Cbl-dependent c-FLIP degradation and sensitivity of TRAIL-induced apoptosis. Cancer Res. 2013, 73, 1946-1957.