Int6/eIF3e is essential for proliferation and survival of human glioblastoma cells

International Journal of Molecular Sciences

Volumn 15, Issue 2, 2014, Pages 2172-2190

  Sesen, Julie ^a   Cammas, Anne ^a   Scotland, Sarah J ^a   Elefterion, Bertand ^a   Lemarié, Anthony ^a   Millevoi, Stefania ^a   Mathew, Lijoy K ^b   Seva, Cathy ^a   Toulas, Christine ^a   Moyal, Elizabeth Cohen Jonathan ^a,c   Skuli, Nicolas ^a  

^a CANCER RESEARCH CENTER OF TOULOUSE   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c INSTITUT CLAUDIUS REGAUD   (France)

Author keywords

Apoptosis; EIF3e; Eukaryotic translation initiation factor; Glioblastoma; Glioma; HIF 1 ; HIF 2 ; Hypoxia inducible factors; Int6; Proliferation

Indexed keywords

ALPHA5 INTEGRIN; CASPASE 3; CASPASE 7; DELTA LIKE LIGAND 4; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INITIATION FACTOR; INITIATION FACTOR 3E; KI 67 ANTIGEN; LIPOCORTIN 5; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEPTIDES AND PROTEINS; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN BAX; PROTEIN BCL 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN; INITIATION FACTOR 3;

APOPTOSIS; ARTICLE; CELL CYCLE G0 PHASE; CELL MIGRATION; CELL PROLIFERATION; CELL PROLIFERATION ASSAY; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENE SILENCING; GLIOBLASTOMA; HUMAN; HUMAN CELL; NONVIRAL GENE DELIVERY SYSTEM; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA TRANSLATION; TUMOR CELL; WESTERN BLOTTING; BIOLOGICAL MODEL; BRAIN TUMOR; CELL CYCLE CHECKPOINT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORTALITY; TUMOR CELL LINE;

APOPTOSIS; BRAIN NEOPLASMS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; EUKARYOTIC INITIATION FACTOR-3; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GLIOBLASTOMA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MODELS, BIOLOGICAL; RNA INTERFERENCE;

EID: 84893166893     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15022172     Document Type: Article

References (45)

1. Tanaka, S.; Louis, D.N.; Curry, W.T.; Batchelor, T.T.; Dietrich, J. Diagnostic and therapeutic avenues for glioblastoma: No longer a dead end? Nat. Rev. Clin. Oncol. 2012, 10, 14-26.
2. Cloughesy, T.F.; Cavenee, W.K.; Mischel, P.S. Glioblastoma: From molecular pathology to targeted treatment. Annu. Rev. Pathol. 2013, doi:10.1146/annurev-pathol-011110-130324.
3. Yang, L.; Lin, C.; Wang, L.; Guo, H.; Wang, X. Hypoxia and hypoxia-inducible factors in glioblastoma multiforme progression and therapeutic implications. Exp. Cell Res. 2012, 318, 2417-2426.
4. Krock, B.L.; Skuli, N.; Simon, M.C. Hypoxia-induced angiogenesis: Good and evil. Genes Cancer 2011, 2, 1117-1133.
5. Keith, B.; Johnson, R.S.; Simon, M.C. Hif1α and hif2α: Sibling rivalry in hypoxic tumour growth and progression. Nat. Rev. Cancer 2012, 12, 9-22.
6. Chen, L.; Endler, A.; Shibasaki, F. Hypoxia and angiogenesis: Regulation of hypoxia-inducible factors via novel binding factors. Exp. Mol. Med. 2009, 41, 849-857.
7. Pietras, A.; Johnsson, A.S.; Pahlman, S. The hif-2α-driven pseudo-hypoxic phenotype in tumor aggressiveness, differentiation, and vascularization. Curr. Top. Microbiol. Immunol. 2010, 345, 1-20.
8. Li, Z.; Bao, S.; Wu, Q.; Wang, H.; Eyler, C.; Sathornsumetee, S.; Shi, Q.; Cao, Y.; Lathia, J.; McLendon, R. E.; et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009, 15, 501-513.
9. Chen, L.; Uchida, K.; Endler, A.; Shibasaki, F. Mammalian tumor suppressor int6 specifically targets hypoxia inducible factor 2α for degradation by hypoxiaand pvhl-independent regulation. J. Biol. Chem. 2007, 282, 12707-12716.
10. Miyashita, R.; Chen, L.; Oshiro, H.; Uchino, H.; Shibasaki, F. Int6 silencing causes induction of angiogenic factors in neuronal cells via accumulation of hypoxia-inducible factor 2α and decreases brain damage in rats. Neurosci. Lett. 2006, 528, 83-88.
11. Chen, L.; Endler, A.; Uchida, K.; Horiguchi, S.; Morizane, Y.; Iijima, O.; Toi, M.; Shibasaki, F. Int6/eif3e silencing promotes functional blood vessel outgrowth and enhances wound healing by upregulating hypoxia-induced factor 2α expression. Circulation 2010, 122, 910-919.
12. Endler, A.; Chen, L.; Li, Q.; Uchida, K.; Hashimoto, T.; Lu, L.; Xu, G.T.; Shibasaki, F. Int6/eif3e silenced hif2α stabilization enhances migration and tube formation of huvecs via IL-6 and IL-8 signaling. Cytokine 2013, 62, 115-122.
13. Silvera, D.; Formenti, S.C.; Schneider, R.J. Translational control in cancer. Nat. Rev. Cancer 2010, 10, 254-266.
14. Hershey, J.W. Regulation of protein synthesis and the role of eif3 in cancer. Br. J. Med. Biol. Res. 2010, 43, 920-930.
15. Damoc, E.; Fraser, C.S.; Zhou, M.; Videler, H.; Mayeur, G.L.; Hershey, J.W.; Doudna, J.A.; Robinson, C.V.; Leary, J.A. Structural characterization of the human eukaryotic initiation factor 3 protein complex by mass spectrometry. Mol. Cell. Proteomics 2007, 6, 1135-1146.
16. Marchione, R.; Leibovitch, S.A.; Lenormand, J.L. The translational factor eif3f: The ambivalent eif3 subunit. Cell. Mol. Life Sci. 2013, 70, 3603-3616.
17. Morris, C.; Tomimatsu, N.; Richard, D.J.; Cluet, D.; Burma, S.; Khanna, K.K.; Jalinot, P. Int6/eif3e interacts with atm and is required for proper execution of the DNA damage response in human cells. Cancer Res. 2012, 72, 2006-2016.
18. Grzmil, M.; Rzymski, T.; Milani, M.; Harris, A.L.; Capper, R.G.; Saunders, N.J.; Salhan, A.; Ragoussis, J.; Norbury, C.J. An oncogenic role of eif3e/int6 in human breast cancer. Oncogene 2010, 29, 4080-4089.
19. Gillis, L.D.; Lewis, S.M. Decreased eif3e/int6 expression causes epithelial-to-mesenchymal transition in breast epithelial cells. Oncogene 2012, 32, 3598-3605.
20. Cappuzzo, F.; Varella-Garcia, M.; Rossi, E.; Gajapathy, S.; Valente, M.; Drabkin, H.; Gemmill, R. Myc and eif3h coamplification significantly improve response and survival of non-small cell lung cancer patients (nsclc) treated with gefitinib. J. Thorac. Oncol. 2009, 4, 472-478.
21. Nupponen, N.N.; Porkka, K.; Kakkola, L.; Tanner, M.; Persson, K.; Borg, A.; Isola, J.; Visakorpi, T. Amplification and overexpression of p40 subunit of eukaryotic translation initiation factor 3 in breast and prostate cancer. Am. J. Pathol. 1999, 154, 1777-1783.
22. Scoles, D.R.; Yong, W.H.; Qin, Y.; Wawrowsky, K.; Pulst, S.M. Schwannomin inhibits tumorigenesis through direct interaction with the eukaryotic initiation factor subunit c (eif3c). Hum. Mol. Genet. 2006, 15, 1059-1070.
23. Liang, H.; Ding, X.; Zhou, C.; Zhang, Y.; Xu, M.; Zhang, C.; Xu, L. Knockdown of eukaryotic translation initiation factors 3b (eif3b) inhibits proliferation and promotes apoptosis in glioblastoma cells. Neurol. Sci. 2012, 33, 1057-1062.
24. Miyazaki, S.; Kozak, C.A.; Marchetti, A.; Buttitta, F.; Gallahan, D.; Callahan, R. The chromosomal location of the mouse mammary tumor gene int6 and related pseudogenes in the mouse genome. Genomics 1995, 27, 420-424.
25. Miyazaki, S.; Imatani, A.; Ballard, L.; Marchetti, A.; Buttitta, F.; Albertsen, H.; Nevanlinna, H.A.; Gallahan, D.; Callahan, R. The chromosome location of the human homolog of the mouse mammary tumor-associated gene int6 and its status in human breast carcinomas. Genomics 1997, 46, 155-158.
26. Buttitta, F.; Martella, C.; Barassi, F.; Felicioni, L.; Salvatore, S.; Rosini, S.; D'Antuono, T.; Chella, A.; Mucilli, F.; Sacco, R.; et al. Int6 expression can predict survival in early-stage non-small cell lung cancer patients. Clin. Cancer Res. 2005, 11, 3198-3204.
27. Umar, A.; Kang, H.; Timmermans, A.M.; Look, M.P.; Meijer-van Gelder, M.E.; den Bakker, M.A.; Jaitly, N.; Martens, J.W.; Luider, T.M.; Foekens, J. A.; et al. Identification of a putative protein profile associated with tamoxifen therapy resistance in breast cancer. Mol. Cell. Proteomics 2009, 8, 1278-1294.
28. Suo, J.; Snider, S.J.; Mills, G.B.; Creighton, C.J.; Chen, A.C.; Schiff, R.; Lloyd, R.E.; Chang, E.C. Int6 regulates both proteasomal degradation and translation initiation and is critical for proper formation of acini by human mammary epithelium. Oncogene 2010, 30, 724-736.
29. Morris, C.; Jalinot, P. Silencing of human int-6 impairs mitosis progression and inhibits cyclin b-cdk1 activation. Oncogene 2005, 24, 1203-1211.
30. Grzmil, M.; Whiting, D.; Maule, J.; Anastasaki, C.; Amatruda, J.F.; Kelsh, R.N.; Norbury, C.J.; Patton, E.E. The int6 cancer gene and mek signaling pathways converge during zebrafish development. PLoS One 2007, 2, e959.
31. Kessler, J.; Hahnel, A.; Wichmann, H.; Rot, S.; Kappler, M.; Bache, M.; Vordermark, D. Hif-1α inhibition by sirna or chetomin in human malignant glioma cells: Effects on hypoxic radioresistance and monitoring via ca9 expression. BMC Cancer 2010, 10, 605.
32. Jensen, R.L.; Ragel, B.T.; Whang, K.; Gillespie, D. Inhibition of hypoxia inducible factor-1α (hif-1α) decreases vascular endothelial growth factor (vegf) secretion and tumor growth in malignant gliomas. J. Neurooncol. 2006, 78, 233-247.
33. Gillespie, D.L.; Whang, K.; Ragel, B.T.; Flynn, J.R.; Kelly, D.A.; Jensen, R.L. Silencing of hypoxia inducible factor-1α by rna interference attenuates human glioma cell growth in vivo. Clin. Cancer Res. 2007, 13, 2441-2448.
34. Franovic, A.; Holterman, C.E.; Payette, J.; Lee, S. Human cancers converge at the hif-2α oncogenic axis. Proc. Natl. Acad. Sci. USA 2009, 106, 21306-21311.
35. Morris, C.; Wittmann, J.; Jack, H.M.; Jalinot, P. Human int6/eif3e is required for nonsense-mediated mrna decay. EMBO Rep. 2007, 8, 596-602.
36. Zhang, X.; Chen, T.; Zhang, J.; Mao, Q.; Li, S.; Xiong, W.; Qiu, Y.; Xie, Q.; Ge, J. Notch1 promotes glioma cell migration and invasion by stimulating β-catenin and NF-κB signaling via akt activation. Cancer Sci. 2012, 103, 181-190.
37. Kil, W.J.; Tofilon, P.J.; Camphausen, K. Post-radiation increase in vegf enhances glioma cell motility in vitro. Radiat. Oncol. 2012, 7, 25.
38. Xu, C.; Wu, X.; Zhu, J. Vegf promotes proliferation of human glioblastoma multiforme stem-like cells through vegf receptor 2. Sci. World J. 2013, 2013, 417413.
39. Nazarenko, I.; Hede, S.M.; He, X.; Hedren, A.; Thompson, J.; Lindstrom, M.S.; Nister, M. Pdgf and pdgf receptors in glioma. Ups. J. Med. Sci. 2012, 117, 99-112.
40. Taga, T.; Suzuki, A.; Gonzalez-Gomez, I.; Gilles, F.H.; Stins, M.; Shimada, H.; Barsky, L.; Weinberg, K.I.; Laug, W.E. αV-integrin antagonist emd 121974 induces apoptosis in brain tumor cells growing on vitronectin and tenascin. Int. J. Cancer 2002, 98, 690-697.
41. MacDonald, T.J.; Ladisch, S. Antisense to integrin alpha v inhibits growth and induces apoptosis in medulloblastoma cells. Anticancer Res. 2001, 21, 3785-3791.
42. Heddleston, J.M.; Li, Z.; McLendon, R.E.; Hjelmeland, A.B.; Rich, J.N. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009, 8, 3274-3284.
43. Heddleston, J.M.; Li, Z.; Lathia, J.D.; Bao, S.; Hjelmeland, A.B.; Rich, J.N. Hypoxia inducible factors in cancer stem cells. Br. J. Cancer 2010, 102, 789-795.
44. Skuli, N.; Monferran, S.; Delmas, C.; Lajoie-Mazenc, I.; Favre, G.; Toulas, C.; Cohen-Jonathan-Moyal, E. Activation of rhob by hypoxia controls hypoxia-inducible factor-1α stabilization through glycogen synthase kinase-3 in u87 glioblastoma cells. Cancer Res. 2006, 66, 482-489.
45. Skuli, N.; Majmundar, A.J.; Krock, B.L.; Mesquita, R.C.; Mathew, L.K.; Quinn, Z.L.; Runge, A.; Liu, L.; Kim, M.N.; Liang, J.; et al. Endothelial hif-2α regulates murine pathological angiogenesis and revascularization processes. J. Clin. Investig. 2012, 122, 1427-1443.