Proteasome inhibition with bortezomib induces cell death in GBM stem-like cells and temozolomide-resistant glioma cell lines, but stimulates GBM stem-like cells' VEGF production and angiogenesis: Laboratory investigation

Journal of Neurosurgery

Volumn 119, Issue 6, 2013, Pages 1415-1423

  Bota, Daniela A ^a   Alexandru, Daniela ^a   Eir, Stephen T K ^b   Bigner, Darell ^b   Vredenburgh, James ^b   Friedman, Henry S ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Bevacizumab; Bortezomib; Glioma; Oncology

Indexed keywords

BEVACIZUMAB; BORTEZOMIB; CASPASE 3; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TEMOZOLOMIDE; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; DRUG ACTIVITY; DRUG EFFECT; ENZYME ACTIVATION; GLIOBLASTOMA; GLIOMA CELL; GLIOMA STEM LIKE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR VOLUME; TUMOR XENOGRAFT;

EID: 84889250555     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2013.7.JNS1323     Document Type: Article

References (37)

1. Adams J: Potential for proteasome inhibition in the treatment of cancer. Drug Discov Today 8:307-315, 2003
2. Adams J, Palombella VJ, Elliott PJ: Proteasome inhibition: a new strategy in cancer treatment. Invest New Drugs 18:109-121, 2000
3. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, et al: Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66:7843-7848, 2006
4. Bektas M, Johnson SP, Poe WE, Bigner DD, Friedman HS: A sphingosine kinase inhibitor induces cell death in temozolomide resistant glioblastoma cells. Cancer Chemother Pharmacol 64:1053-1058, 2009
5. Bianchi G, Oliva L, Cascio P, Pengo N, Fontana F, Cerruti F, et al: The proteasome load versus capacity balance determines apoptotic sensitivity of multiple myeloma cells to proteasome inhibition. Blood 113:3040-3049, 2009
6. Chang CJ, Sun CH, Liaw LH, Berns MW, Nelson JS: In vitro and in vivo photosensitizing capabilities of 5-ALA versus photofrin in vascular endothelial cells. Lasers Surg Med 24: 178-186, 1999
7. Ciechanover A, Orian A, Schwartz AL: The ubiquitin-mediated proteolytic pathway: mode of action and clinical implications. J Cell Biochem Suppl 34:40-51, 2000
8. Friedman HS, Houghton PJ, Schold SC, Keir S, Bigner DD: Activity of 9-dimethylaminomethyl-10-hydroxycamptothecin against pediatric and adult central nervous system tumor xenografts. Cancer Chemother Pharmacol 34:171-174, 1994
9. Friedman HS, Kerby T, Calvert H: Temozolomide and treatment of malignant glioma. Clin Cancer Res 6:2585-2597, 2000
10. Fujioka S, Schmidt C, Sclabas GM, Li Z, Pelicano H, Peng B, et al: Stabilization of p53 is a novel mechanism for proapoptotic function of NF-kappaB. J Biol Chem 279:27549-27559, 2004
11. Gong X, Schwartz PH, Linskey ME, Bota DA: Neural stem/progenitors and glioma stem-like cells have differential sensitivity to chemotherapy. Neurology 76:1126-1134, 2011
12. Hegi ME, Diserens AC, Godard S, Dietrich PY, Regli L, Ostermann S, et al: Clinical trial substantiates the predictive value of O-6-methylguanine-DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin Cancer Res 10:1871-1874, 2004
13. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al: MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997-1003, 2005
14. Hemeryck A, Geerts R, Monbaliu J, Hassler S, Verhaeghe T, Diels L, et al: Tissue distribution and depletion kinetics of bortezomib and bortezomib-related radioactivity in male rats after single and repeated intravenous injection of 14 C-bortezomib. Cancer Chemother Pharmacol 60:777-787, 2007
15. Hough R, Pratt G, Rechsteiner M: Ubiquitin-lysozyme conjugates. Identification and characterization of an ATP-dependent protease from rabbit reticulocyte lysates. J Biol Chem 261:2400-2408, 1986
16. Houghton PJ, Morton CL, Kolb EA, Lock R, Carol H, Reynolds CP, et al: Initial testing (stage 1) of the proteasome inhibitor bortezomib by the pediatric preclinical testing program. Pediatr Blood Cancer 50:37-45, 2008
17. Jensen RL, Ragel BT, Whang K, Gillespie D: Inhibition of hypoxia inducible factor-1alpha (HIF-1alpha) decreases vascular endothelial growth factor (VEGF) secretion and tumor growth in malignant gliomas. J Neurooncol 78:233-247, 2006
18. Kim S, Choi K, Kwon D, Benveniste EN, Choi C: Ubiquitin-proteasome pathway as a primary defender against TRAIL-mediated cell death. Cell Mol Life Sci 61:1075-1081, 2004
19. Koepp DM, Harper JW, Elledge SJ: How the cyclin became a cyclin: regulated proteolysis in the cell cycle. Cell 97:431-434, 1999
20. Labussiere M, Pinel S, Delfortrie S, Plenat F, Chastagner P: Proteasome inhibition by bortezomib does not translate into efficacy on two malignant glioma xenografts. Oncol Rep 20: 1283-1287, 2008
21. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, et al: Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67, 2006
22. Phuphanich S, Supko JG, Carson KA, Grossman SA, Burt Nabors L, Mikkelsen T, et al: Phase 1 clinical trial of bortezomib in adults with recurrent malignant glioma. J Neurooncol 100:95-103, 2010
23. Pistollato F, Chen HL, Rood BR, Zhang HZ, D'Avella D, Denaro L, et al: Hypoxia and HIF1alpha repress the differentiative effects of BMPs in high-grade glioma. Stem Cells 27:7-17, 2009
24. Ri M, Iida S, Nakashima T, Miyazaki H, Mori F, Ito A, et al: Bortezomib-resistant myeloma cell lines: a role for mutated PSMB5 in preventing the accumulation of unfolded proteins and fatal ER stress. Leukemia 24:1506-1512, 2010
25. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352: 987-996, 2005
26. Taniguchi E, Cho MJ, Arenkiel BR, Hansen MS, Rivera OJ, McCleish AT, et al: Bortezomib reverses a post-translational mechanism of tumorigenesis for patched1 haploinsufficiency in medulloblastoma. Pediatr Blood Cancer 53:136-144, 2009
27. Veschini L, Belloni D, Foglieni C, Cangi MG, Ferrarini M, Caligaris-Cappio F, et al: Hypoxia-inducible transcription factor-1 alpha determines sensitivity of endothelial cells to the proteosome inhibitor bortezomib. Blood 109:2565-2570, 2007
28. Vlashi E, Pajonk F: Targeted cancer stem cell therapies start with proper identification of the target. Mol Cancer Res 8:291, 2010 (Letter)
29. Vredenburgh JJ, Desjardins A, Herndon JE II, Marcello J, Reardon DA, Quinn JA, et al: Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 25:4722-4729, 2007
30. Wagenknecht B, Hermisson M, Groscurth P, Liston P, Krammer PH, Weller M: Proteasome inhibitor-induced apoptosis of glioma cells involves the processing of multiple caspases and cytochrome c release. J Neurochem 75:2288-2297, 2000
31. Wang CY, Mayo MW, Baldwin AS Jr: TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274:784-787, 1996
32. Wen PY, Kesari S: Malignant gliomas in adults. N Engl J Med 359:492-507, 2008
33. Williams S, Pettaway C, Song R, Papandreou C, Logothetis C, McConkey DJ: Differential effects of the proteasome inhibitor bortezomib on apoptosis and angiogenesis in human prostate tumor xenografts. Mol Cancer Ther 2:835-843, 2003
34. Williams SA, McConkey DJ: The proteasome inhibitor bortezomib stabilizes a novel active form of p53 in human LNCaP-Pro5 prostate cancer cells. Cancer Res 63:7338-7344, 2003
35. Yang Y, Yu X: Regulation of apoptosis: the ubiquitous way. FASEB J 17:790-799, 2003
36. Yin D, Zhou H, Kumagai T, Liu G, Ong JM, Black KL, et al: Proteasome inhibitor PS-341 causes cell growth arrest and apoptosis in human glioblastoma multiforme (GBM). Oncogene 24:344-354, 2005
37. Zhu K, Dunner K Jr, McConkey DJ: Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells. Oncogene 29:451-462, 2010