Anti-neoplastic activity of low-dose endothelial-monocyte activating polypeptide-II results from defective autophagy and G2/M arrest mediated by PI3K/Akt/FoxO1 axis in human glioblastoma stem cells

Biochemical Pharmacology

Volumn 89, Issue 4, 2014, Pages 477-489

  Liu, Jing ^a   Liu, Libo ^a   Xue, Yixue ^a   Meng, Fanjie ^a   Li, Shuai ^a   Wang, Ping ^a   Liu, Yunhui ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Atg2B; Autophagy; EMAP II; FoxO1; GSCs

Indexed keywords

3 METHYLADENINE; ENDOTHELIAL MONOCYTE ACTIVATING POLYPEPTIDE II; EPIDERMAL GROWTH FACTOR; FAT DROPLET; FIBROBLAST GROWTH FACTOR 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER INHIBITION; CANCER STEM CELL; CELL VIABILITY; CELL VIABILITY ASSAY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOTOXICITY; FLOW CYTOMETRY; G2 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; TRANSMISSION ELECTRON MICROSCOPY; TUMOR GROWTH; TUMOR VASCULARIZATION; TUMOR VOLUME; TUMOR XENOGRAFT;

3-METHYLADENINE (PUBCHEM CID: 1673); ATG2B; AUTOPHAGY; EMAP-II; FOXO1; GSCS; INSULIN-LIKE GROWTH FACTOR-1 (PUBCHEM CID: 44134783);

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; BRAIN NEOPLASMS; CELL LINE, TUMOR; CYTOKINES; FORKHEAD TRANSCRIPTION FACTORS; G2 PHASE; GLIOBLASTOMA; HUMANS; MALE; MICE; MICE, NUDE; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASE; RANDOM ALLOCATION; RECOMBINANT PROTEINS; RNA INTERFERENCE; RNA-BINDING PROTEINS; SECOND MESSENGER SYSTEMS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901592475     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.04.014     Document Type: Article

References (49)

1. B.B. Zhou, H. Zhang, M. Damelin, K.G. Geles, J.C. Grindley, and P.B. Dirks Tumour-initiating cells: challenges and opportunities for anticancer drug discovery Nat Rev Drug Discovery 8 2009 806 823
2. M. Nakada, S. Nakada, T. Demuth, N.L. Tran, D.B. Hoelzinger, and M.E. Berens Molecular targets of glioma invasion Cell Mol Life Sci: CMLS 64 2007 458 478
3. S.K. Singh, C. Hawkins, I.D. Clarke, J.A. Squire, J. Bayani, and T. Hide et al. Identification of human brain tumour initiating cells Nature 432 2004 396 401 (Pubitemid 39551674)
4. I. Nakano, and H.I. Kornblum Brain tumor stem cells Pediatric Res 59 2006 54R 58R (Pubitemid 43740036)
5. S.K. Singh, I.D. Clarke, M. Terasaki, V.E. Bonn, C. Hawkins, and J. Squire et al. Identification of a cancer stem cell in human brain tumors Cancer Res 63 2003 5821 5828 (Pubitemid 37187480)
6. R. Galli, E. Binda, U. Orfanelli, B. Cipelletti, A. Gritti, and S. De Vitis et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma Cancer Res 64 2004 7011 7021 (Pubitemid 39331011)
7. J. Kao, K. Houck, Y. Fan, I. Haehnel, S.K. Libutti, and M.L. Kayton et al. Characterization of a novel tumor-derived cytokine. Endothelial-monocyte activating polypeptide II J Biol Chem 269 1994 25106 25119
8. T.G. Nuhrenberg, N. Langwieser, J.B. Schwarz, Y. Hou, P. Frank, and F. Sorge et al. EMAP-II downregulation contributes to the beneficial effects of rapamycin after vascular injury Cardiovasc Res 77 2008 580 589 (Pubitemid 351197667)
9. H. Xie, Y.X. Xue, L.B. Liu, and Y.H. Liu Endothelial-monocyte-activating polypeptide II increases blood-tumor barrier permeability by down-regulating the expression levels of tight junction associated proteins Brain Res 1319 2010 13 20
10. R.E. Schwarz, N. Awasthi, S. Konduri, L. Caldwell, D. Cafasso, and M.A. Schwarz Antitumor effects of EMAP II against pancreatic cancer through inhibition of fibronectin-dependent proliferation Cancer Biol Ther 9 2010 632 639
11. M.A. Schwarz, J. Kandel, J. Brett, J. Li, J. Hayward, and R.E. Schwarz et al. Endothelial-monocyte activating polypeptide II, a novel antitumor cytokine that suppresses primary and metastatic tumor growth and induces apoptosis in growing endothelial cells J Exp Med 190 1999 341 354
12. R.E. Schwarz, and M.A. Schwarz In vivo therapy of local tumor progression by targeting vascular endothelium with EMAP-II J Surg Res 120 2004 64 72 (Pubitemid 38686531)
13. L. Crippa, A. Gasparri, A. Sacchi, E. Ferrero, F. Curnis, and A. Corti Synergistic damage of tumor vessels with ultra low-dose endothelial-monocyte activating polypeptide-II and neovasculature-targeted tumor necrosis factor-alpha Cancer Res 68 2008 1154 1161 (Pubitemid 351272234)
14. A.C. Berger, H.R. Alexander, G. Tang, P.S. Wu, S.M. Hewitt, and E. Turner et al. Endothelial monocyte activating polypeptide II induces endothelial cell apoptosis and may inhibit tumor angiogenesis Microvasc Res 60 2000 70 80 (Pubitemid 30456829)
15. A.V. Knizhnik, W.P. Roos, T. Nikolova, S. Quiros, K.H. Tomaszowski, and M. Christmann et al. Survival and death strategies in glioma cells: autophagy, senescence and apoptosis triggered by a single type of temozolomide-induced DNA damage PLoS One 8 2013 e55665
16. G. Kroemer, and B. Levine Autophagic cell death: the story of a misnomer Nat Rev Mol Cell Biol 9 2008 1004 1010
17. M. Salazar, A. Carracedo, I.J. Salanueva, S. Hernandez-Tiedra, M. Lorente, and A. Egia et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells J Clin Invest 119 2009 1359 1372
18. R. Mathew, S. Kongara, B. Beaudoin, C.M. Karp, K. Bray, and K. Degenhardt et al. Autophagy suppresses tumor progression by limiting chromosomal instability Genes Dev 21 2007 1367 1381 (Pubitemid 46871040)
19. R. Guo, and J. Ren Deficiency in AMPK attenuates ethanol-induced cardiac contractile dysfunction through inhibition of autophagosome formation Cardiovasc Res 94 2012 480 491
20. R.A. Gottlieb, and R.M. Mentzer Autophagy during cardiac stress: joys and frustrations of autophagy Annu Rev Physiol 72 2010 45 59
21. J. Lim, Y. Lee, S. Jung, M.B. Youdim, and Y.J. Oh Impaired autophagic flux is critically involved in drug-induced dopaminergic neuronal death Parkinsonism Relat Disord 20 Suppl 1 2014 S162 S166
22. A. van der Horst, and B.M. Burgering Stressing the role of FoxO proteins in lifespan and disease Nat Rev Mol Cell Biol 8 2007 440 450 (Pubitemid 46809159)
23. G. Juhasz, L.G. Puskas, O. Komonyi, B. Erdi, P. Maroy, and T.P. Neufeld et al. Gene expression profiling identifies FKBP39 as an inhibitor of autophagy in larval Drosophila fat body Cell Death Differ 14 2007 1181 1190 (Pubitemid 46794922)
24. C. Mammucari, G. Milan, V. Romanello, E. Masiero, R. Rudolf, and P. Del Piccolo et al. FoxO3 controls autophagy in skeletal muscle in vivo Cell Metab 6 2007 458 471 (Pubitemid 350163055)
25. J. Zhao, J.J. Brault, A. Schild, P. Cao, M. Sandri, and S. Schiaffino et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells Cell Metab 6 2007 472 483 (Pubitemid 350163056)
26. A.K. Velikkakath, T. Nishimura, E. Oita, N. Ishihara, and N. Mizushima Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets Mol Biol Cell 23 2012 896 909
27. Y. Hong, M. Sang, C. Shang, Y.X. Xue, and Y.H. Liu Quantitative analysis of topoisomerase II alpha and evaluation of its effects on cell proliferation and apoptosis in glioblastoma cancer stem cells Neurosci Lett 518 2012 138 143
28. V. Tong, X.W. Teng, T.K. Chang, and F.S. Abbott Valproic acid II: effects on oxidative stress, mitochondrial membrane potential, and cytotoxicity in glutathione-depleted rat hepatocytes Toxicol Sci 86 2005 436 443 (An Official Journal of the Society of Toxicology) (Pubitemid 41418656)
29. T. Kanzawa, I.M. Germano, T. Komata, H. Ito, Y. Kondo, and S. Kondo Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells Cell Death Differ 11 2004 448 457 (Pubitemid 38489422)
30. M.A. Schwarz, H. Zheng, J. Liu, S. Corbett, and R.E. Schwarz Endothelial-monocyte activating polypeptide II alters fibronectin based endothelial cell adhesion and matrix assembly via alpha5 beta1 integrin Exp Cell Res 311 2005 229 239 (Pubitemid 41636316)
31. Z. Li, Y.H. Liu, Y.X. Xue, L.B. Liu, and P. Wang Signal mechanisms underlying low-dose endothelial monocyte-activating polypeptide-II-induced opening of the blood-tumor barrier J Mol Neurosci: MN 48 2012 291 301
32. M. Komatsu, S. Waguri, M. Koike, Y.S. Sou, T. Ueno, and T. Hara et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice Cell 131 2007 1149 1163 (Pubitemid 350235021)
33. R. Lock, S. Roy, C.M. Kenific, J.S. Su, E. Salas, and S.M. Ronen et al. Autophagy facilitates glycolysis during Ras-mediated oncogenic transformation Mol Biol Cell 22 2011 165 178
34. N. Mizushima, and D.J. Klionsky Protein turnover via autophagy: implications for metabolism Annu Rev Nutr 27 2007 19 40 (Pubitemid 351373346)
35. R. Singh, S. Kaushik, Y. Wang, Y. Xiang, I. Novak, and M. Komatsu et al. Autophagy regulates lipid metabolism Nature 458 2009 1131 1135
36. G. Bjorkoy, T. Lamark, A. Brech, H. Outzen, M. Perander, and A. Overvatn et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death J Cell Biol 171 2005 603 614 (Pubitemid 41668720)
37. L. Haataja, T. Gurlo, C.J. Huang, and P.C. Butler Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis Endocr Rev 29 2008 303 316 (Pubitemid 351679701)
38. A. Brunet, A. Bonni, M.J. Zigmond, M.Z. Lin, P. Juo, and L.S. Hu et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor Cell 96 1999 857 868 (Pubitemid 29165088)
39. K. Katayama, A. Nakamura, Y. Sugimoto, T. Tsuruo, and N. Fujita FOXO transcription factor-dependent p15(INK4b) and p19(INK4d) expression Oncogene 27 2008 1677 1686 (Pubitemid 351380267)
40. J. Seoane, H.V. Le, L. Shen, S.A. Anderson, and J. Massague Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation Cell 117 2004 211 223 (Pubitemid 38496241)
41. D. Ramljak, R.J. Calvert, P.W. Wiesenfeld, B.A. Diwan, B. Catipovic, and W.F. Marasas et al. A potential mechanism for fumonisin B(1)-mediated hepatocarcinogenesis: cyclin D1 stabilization associated with activation of Akt and inhibition of GSK-3beta activity Carcinogenesis 21 2000 1537 1546 (Pubitemid 30601646)
42. C.Y. Huang, C.Y. Chan, I.T. Chou, C.H. Lien, H.C. Hung, and M.F. Lee Quercetin induces growth arrest through activation of FOXO1 transcription factor in EGFR-overexpressing oral cancer cells J Nutr Biochem 24 2013 1596 1603
43. K. Fujiwara, E. Iwado, G.B. Mills, R. Sawaya, S. Kondo, and Y. Kondo Akt inhibitor shows anticancer and radiosensitizing effects in malignant glioma cells by inducing autophagy Int J Oncol 31 2007 753 760
44. A. Sengupta, J.D. Molkentin, and K.E. Yutzey FoxO transcription factors promote autophagy in cardiomyocytes J Biol Chem 284 2009 28319 28331
45. Y. Zhao, J. Yang, W. Liao, X. Liu, H. Zhang, and S. Wang et al. Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity Nat Cell Biol 12 2010 665 675
46. A.A. Goldberg, S.D. Bourque, P. Kyryakov, T. Boukh-Viner, C. Gregg, and A. Beach et al. A novel function of lipid droplets in regulating longevity Biochem Soc Trans 37 2009 1050 1055
47. S.D. Kohlwein, M. Veenhuis, and I.J. van der Klei Lipid droplets and peroxisomes: key players in cellular lipid homeostasis or a matter of fat - store 'em up or burn' em down Genetics 193 2013 1 50
48. S. Sheibani, V.R. Richard, A. Beach, A. Leonov, R. Feldman, and S. Mattie et al. Macromitophagy, neutral lipids synthesis, and peroxisomal fatty acid oxidation protect yeast from liponecrosis, a previously unknown form of programmed cell death Cell Cycle 13 2014 138 147
49. K. Athenstaedt, and G. Daum The life cycle of neutral lipids: synthesis, storage and degradation Cell Mol Life Sci: CMLS 63 2006 1355 1369 (Pubitemid 43939017)