Momordin Ic couples apoptosis with autophagy in human hepatoblastoma cancer cells by reactive oxygen species (ROS)-mediated PI3K/Akt and MAPK signaling pathways

Free Radical Biology and Medicine

Volumn 90, Issue , 2016, Pages 230-242

  Mi, Yashi ^a   Xiao, Chunxia ^a   Du, Qingwei ^b   Wu, Wanqiang ^a   Qi, Guoyuan ^a   Liu, Xuebo ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b Functional Food Engineering and Technology Research Center of Shaanxi Province   (China)

Author keywords

Apoptosis; Autophagy; Crosstalk; HepG2 cells; Momordin Ic

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; ANTINEOPLASTIC AGENT; ANTIOXIDANT; BECLIN 1; CASPASE 3; CASPASE 8; CYTOCHROME C; DANSYLCADAVERINE; FAS ANTIGEN; FAS LIGAND; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JANUS KINASE; LAMIN B; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MOMORDIN IC; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; RAPAMYCIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; MOMORDIN I (OLEANOLIC ACID); OLEANOLIC ACID;

APOPTOSIS; ARTICLE; AUTOPHAGY; ENZYME ACTIVATION; HEPATOBLASTOMA; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LIVER CELL CARCINOMA; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; CELL PROLIFERATION; DRUG EFFECTS; HEP-G2 CELL LINE; LIVER NEOPLASMS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

APOPTOSIS; AUTOPHAGY; CELL PROLIFERATION; HEP G2 CELLS; HEPATOBLASTOMA; HUMANS; LIVER NEOPLASMS; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; OLEANOLIC ACID; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES;

EID: 84949239041     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.11.022     Document Type: Article

References (57)

1. A. Jemal, F. Bray, M.M. Center, J. Ferlay, E. Ward, and D. Forman Global cancer statistics CA Cancer J. Clin. 61 2011 69 90
2. C.C. Chiu, J.J. Wang, Y.S. Chen, J.J. Chen, T.C. Tsai, C.C. Lai, D.P. Sun, and H.Y. Shi Trends and predictors of outcomes after surgery for hepatocellular carcinoma: a nationwide population-based study in Taiwan Eur. J. Surg. Oncol (EJSO) 2015 10.1016/j.ejso.2015.04.023
3. A. Nagasaka, K. Kawane, H. Yoshida, and S. Nagata Apaf-1-independent programmed cell death in mouse development Cell Death Differ. 17 2010 931 941
4. D.J. Burgess Apoptosis: refined and lethal Nat. Rev. Cancer 13 2013 79
5. R.L. Deter, P. Baudhuin, and C. De Duve Participation of lysosomes in cellular autophagy induced in rat liver by glucagon J. Cell Biol. 35 1967 C11 C16
6. B. Levine, and J. Yuan Autophagy in cell death: an innocent convict? J. Clin. Investig. 115 2005 2679 2688
7. A. Eisenberg-Lerner, S. Bialik, H.U. Simon, and A. Kimchi Life and death partners: apoptosis, autophagy and the cross-talk between them Cell Death Differ. 16 2009 966 975
8. S. Mukhopadhyay, P.K. Panda, N. Sinha, D.N. Das, and S.K. Bhutia Autophagy and apoptosis: where do they meet? Apoptosis 19 2014 555 566
9. H. Matsuda, Y. Li, J. Yamahara, and M. Yoshikawa Inhibition of gastric emptying by triterpene saponin, momordin Ic, in mice: roles of blood glucose, capsaicin-sensitive sensory nerves, and central nervous system J. Pharmacol. Exp. Ther. 289 1999 729 734
10. H. Matsuda, Y. Li, and M. Yoshikawa Roles of capsaicin-sensitive sensory nerves, endogenous nitric oxide, sulfhydryls, and prostaglandins in gastroprotection by momordin Ic, an oleanolic acid oligoglycoside, on ethanol-induced gastric mucosal lesions in rats Life Sci. 65 1999 PL27 PL32
11. N.Y. Kim, M.K. Lee, M.J. Park, S.J. Kim, H.J. Park, J.W. Choi, S.H. Kim, S.Y. Cho, and J.S. Lee Momordin Ic and oleanolic acid from Kochiae Fructus reduce carbon tetrachloride-induced hepatotoxicity in rats J. Med. Food 8 2005 177 183
12. J. Wang, L. Yuan, H. Xiao, C. Xiao, Y. Wang, and X. Liu Momordin Ic induces HepG2 cell apoptosis through MAPK and PI3K/Akt-mediated mitochondrial pathways Apoptosis 18 2013 751 765
13. F. Nie, X. Zhang, Q. Qi, L. Yang, Y. Yang, W. Liu, N. Lu, Z. Wu, Q. You, and Q. Guo Reactive oxygen species accumulation contributes to gambogic acid-induced apoptosis in human hepatoma SMMC-7721 cells Toxicology 260 2009 60 67
14. C.C. Liu, and J.M. Gebicki Intracellular GSH and ascorbate inhibit radical-induced protein chain peroxidation in HL-60 cells Free Radic. Biol. Med. 52 2012 420 426
15. Z. Liu, G. Song, C. Zou, G. Liu, W. Wu, T. Yuan, and X. Liu Acrylamide induces mitochondrial dysfunction and apoptosis in BV-2 microglial cells Free Radic. Biol. Med. 84 2015 42 53
16. W.S. Lee, R.J. Chen, Y.J. Wang, H. Tseng, J.H. Jeng, S.Y. Lin, Y.C. Liang, C.H. Chen, C.H. Lin, J.K. Lin, P.Y. Ho, J.S. Chu, W.L. Ho, L.C. Chen, and Y.S. Ho In vitro and in vivo studies of the anticancer action of terbinafine in human cancer cell lines: G0/G1 p53-associated cell cycle arrest Int. J. Cancer 106 2003 125 137
17. H.U. Simon, A. Haj-Yehia, and F. Levi-Schaffer Role of reactive oxygen species (ROS) in apoptosis induction Apoptosis 5 2000 415 418
18. M.B. Azad, Y. Chen, and S.B. Gibson Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment Antioxid. Redox Signal. 11 2009 777 790
19. L.C. Cantley The phosphoinositide 3-kinase pathway Science 296 2002 1655 1657
20. W.E. Naugler, and M. Karin NF-kappaB and cancer-identifying targets and mechanisms Curr. Opin. Genet. Dev. 18 2008 19 26
21. E. Vequaud, C. Seveno, D. Loussouarn, L. Engelhart, M. Campone, P. Juin, and S. Barille-Nion YM155 potently triggers cell death in breast cancer cells through an autophagy-NF-kB network Oncotarget 6 2015 13476 13486
22. R.A. Hill, and J.D. Connolly Triterpenoids Nat. Prod. Rep. 30 2013 1028 1065
23. O.O. Elekofehinti Saponins: anti-diabetic principles from medicinal plants - a review Pathophysiology 22 2015 95 103
24. J.M.R. Patlolla, and C.V. Rao Anti-inflammatory and anti-cancer properties of β-Escin, a triterpene saponin Curr. Pharmacol. Rep. 1 2015 170 178
25. J. Zong, R. Wang, G. Bao, T. Ling, L. Zhang, X. Zhang, and R. Hou Novel triterpenoid saponins from residual seed cake of Camellia oleifera Abel. show anti-proliferative activity against tumor cells Fitoterapia 104 2015 7 13
26. L.T. Han, J. Li, F. Huang, S.G. Yu, and N.B. Fang Triterpenoid saponins from Anemone flaccida induce apoptosis activity in HeLa cells J. Asian Nat. Prod. Res. 11 2009 122 127
27. R.S. Sloviter Apoptosis: a guide for the perplexed Trends Pharmacol. Sci. 23 2002 19 24
28. A.J. Meijer, and P. Codogno Regulation and role of autophagy in mammalian cells Int. J. Biochem. Cell Biol. 36 2004 2445 2462
29. S. Shen, O. Kepp, M. Michaud, I. Martins, H. Minoux, D. Metivier, M.C. Maiuri, R.T. Kroemer, and G. Kroemer Association and dissociation of autophagy, apoptosis and necrosis by systematic chemical study Oncogene 30 2011 4544 4556
30. G.J. Laurent Autophagy: too much or too little recycling in the cell? Int. J. Biochem. Cell Biol. 36 2004 2364
31. W. Chaabane, S.D. User, M. El-Gazzah, R. Jaksik, E. Sajjadi, J. Rzeszowska-Wolny, and M.J. Los Autophagy, apoptosis, mitoptosis and necrosis: interdependence between those pathways and effects on cancer Arch. Immunol. Ther. Exp. (Warsz) 61 2013 43 58
32. X.H. Liang, L.K. Kleeman, H.H. Jiang, G. Gordon, J.E. Goldman, G. Berry, B. Herman, and B. Levine Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein J. Virol. 72 1998 8586 8596
33. Y. Kabeya, N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori LC-3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing EMBO J. 19 2000 5720 5728
34. N. Mizushima Methods for monitoring autophagy Int. J. Biochem. Cell Biol. 36 2004 2491 2502
35. I. Tanida, T. Ueno, and E. Kominami LC-3 conjugation system in mammalian autophagy Int. J. Biochem. Cell Biol. 36 2004 2503 2518
36. C. He, and B. Levine The Beclin 1 interactome Curr. Opin. Cell Biol. 22 2010 140 149
37. J. Thorburn, F. Moore, A. Rao, W.W. Barclay, L.R. Thomas, K.W. Grant, S.D. Cramer, and A. Thorburn Selective inactivation of a Fas-associated death domain protein (FADD)-dependent apoptosis and autophagy pathway in immortal epithelial cells Mol. Biol. Cell 16 2005 1189 1199
38. W.J. Guo, Y.M. Zhang, L. Zhang, B. Huang, F.F. Tao, W. Chen, Z.J. Guo, Q. Xu, and Y. Sun Novel monofunctional platinum (II) complex mono-Pt induces apoptosis-independent autophagic cell death in human ovarian carcinoma cells, distinct from cisplatin Autophagy 9 2013 996 1008
39. R.J. Chen, C.T. Ho, and Y.J. Wang Pterostilbene induces autophagy and apoptosis in sensitive and chemoresistant human bladder cancer cells Mol. Nutr. Food Res. 54 2010 1819 1832
40. M.J. Abedin, D. Wang, M.A. McDonnell, U. Lehmann, and A. Kelekar Autophagy delays apoptotic death in breast cancer cells following DNA damage Cell Death Differ. 14 2007 500 510
41. L.U. Ling, K.B. Tan, H. Lin, and G.N. Chiu The role of reactive oxygen species and autophagy in safingol-induced cell death Cell Death Dis. 2 2011 e129
42. G.M. Fimia, and M. Piacentini Regulation of autophagy in mammals and its interplay with apoptosis Cell. Mol. Life Sci. 67 2010 1581 1588
43. Y. Zhan, K. Gong, C. Chen, H. Wang, and W. Li P38 MAP kinase functions as a switch in MS-275-induced reactive oxygen species-dependent autophagy and apoptosis in human colon cancer cells Free Radic. Biol. Med. 53 2012 532 543
44. B.N. Singh, D. Kumar, S. Shankar, and R.K. Srivastava Rottlerin induces autophagy which leads to apoptotic cell death through inhibition of PI3K/Akt/mTOR pathway in human pancreatic cancer stem cells Biochem. Pharmacol. 84 2012 1154 1163
45. M.C. Maiuri, E. Zalckvar, A. Kimchi, and G. Kroemer Self-eating and self-killing: crosstalk between autophagy and apoptosis Nat. Rev. Mol. Cell Biol. 8 2007 741 752
46. A. Kumar, V. Rajendran, R. Sethumadhavan, and R. Purohit AKT kinase pathway: a leading target in cancer research Sci. World J. 2013 2013 756134
47. D.J. Klionsky, and S.D. Emr Autophagy as a regulated pathway of cellular degradation Science 290 2000 1717 1721
48. A.A. Ellington, M.A. Berhow, and K.W. Singletary Inhibition of Akt signaling and enhanced ERK1/2 activity are involved in induction of macroautophagy by triterpenoid B-group soyasaponins in colon cancer cells Carcinogenesis 27 2006 298 306
49. K.J. Park, S.H. Lee, C.H. Lee, J.Y. Jang, J. Chung, M.H. Kwon, and Y.S. Kim Upregulation of Beclin-1 expression and phosphorylation of Bcl-2 and p53 are involved in the JNK-mediated autophagic cell death Biochem. Biophys. Res. Commun. 382 2009 726 729
50. G. Tang, Z. Yue, Z. Talloczy, T. Hagemann, W. Cho, A. Messing, D.L. Sulzer, and J.E. Goldman Autophagy induced by Alexander disease-mutant GFAP accumulation is regulated by p38/MAPK and mTOR signaling pathways Hum. Mol. Genet. 17 2008 1540 1555
51. J. Fortun, W.A. Dunn Jr., S. Joy, J. Li, and L. Notterpek Emerging role for autophagy in the removal of aggresomes in Schwann cells J. Neurosci. 23 2003 10672 10680
52. Y. Wang, and Z.H. Qin Molecular and cellular mechanisms of excitotoxic neuronal death Apoptosis 15 2010 1382 1402
53. M. Djavaheri-Mergny, M. Amelotti, J. Mathieu, F. Besancon, C. Bauvy, and P. Codogno Regulation of autophagy by NFkappaB transcription factor and reactives oxygen species Autophagy 3 2007 390 392
54. A. Salminen, J.M. Hyttinen, A. Kauppinen, and K. Kaarniranta Context-dependent regulation of autophagy by IKK-NF-kappaB signaling: impact on the aging process Int. J. Cell Biol. 2012 2012 849541
55. C. Nakanishi, and M. Toi Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs Nat. Rev. Cancer 5 2005 297 309
56. H.C. Dan, M.J. Cooper, P.C. Cogswell, J.A. Duncan, J.P.-Y. Ting, and A.S. Baldwin Akt-dependent regulation of NF-κB is controlled by mTOR and Raptor in association with IKK Genes Dev. 22 2008 1490 1500
57. H.R. Wong, M. Ryan, and J.R. Wispé The heat shock response inhibits inducible nitric oxide synthase gene expression by blocking Iκ-B degradation and NF-κB nuclear translocation Biochem. Biophys. Res. Commun. 231 1997 257 263