Targeting apoptosis pathways in glioblastoma

Cancer Letters

Volumn 332, Issue 2, 2013, Pages 335-345

  Eisele, Günter ^a   Weller, Michael ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Apoptosis; Glioblastoma; Targeted therapy

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANTINEOPLASTIC AGENT; APOPTOSIS INDUCING FACTOR; AT 406; BORTEZOMIB; CASPASE; CISPLATIN; DEATH RECEPTOR; ERLOTINIB; FAS LIGAND; GOSSYPOL; GROWTH FACTOR; HYDROXYUREA; IMATINIB; INHIBITOR OF APOPTOSIS PROTEIN; NAVITOCLAX; NIMUSTINE; PROTEASOME INHIBITOR; PROTEIN BCL 2; PROTEIN P53; RAPAMYCIN; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; ROTTLERIN; SC 68896; SORAFENIB; TEMOZOLOMIDE; TEMSIROLIMUS; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANDETANIB;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG TARGETING; ENZYME ACTIVATION; GLIOBLASTOMA; HEMATOLOGIC MALIGNANCY; HUMAN; INTRACELLULAR SIGNALING; LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; SOLID TUMOR;

EID: 84876093748     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.12.012     Document Type: Review

References (147)

1. Ohgaki H., Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J. Neuropathol. Exp. Neurol. 2005, 64:479-489.
2. Adamson C., Kanu O.O., Mehta A.I., Di C., Lin N., Mattox A.K., et al. Glioblastoma multiforme: a review of where we have been and where we are going. Expert Opin. Invest. Drugs 2009, 18:1061-1083.
3. Garcia-Barros M., Paris F., Cordon-Cardo C., Lyden D., Rafii S., Haimovitz-Friedman A., et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003, 300:1155-1159.
4. Kioi M., Vogel H., Schultz G., Hoffman R.M., Harsh G.R., Brown J.M. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest. 2010, 120:694-705.
5. Schiffer D., Cavalla P., Migheli A., Chio A., Giordana M.T., Marino S., et al. Apoptosis and cell proliferation in human neuroepithelial tumors. Neurosci. Lett. 1995, 195:81-84.
6. Ribeiro Mde C., Coutinho L.M., Hilbig A. The role of apoptosis, cell proliferation index, bcl-2, and p53 in glioblastoma prognosis. Arq. Neuropsiquiatra 2004, 62:262-270.
7. Korshunov A., Golanov A., Sycheva R., Pronin I. Prognostic value of tumour associated antigen immunoreactivity and apoptosis in cerebral glioblastomas: an analysis of 168 cases. J. Clin. Pathol. 1999, 52:574-580.
8. Kuriyama H., Lamborn K.R., O'Fallon J.R., Iturria N., Sebo T., Schaefer P.L., et al. Prognostic significance of an apoptotic index and apoptosis/proliferation ratio for patients with high-grade astrocytomas. Neuro-Oncology 2002, 4:179-186.
9. Vogelbaum M.A., Berkey B., Peereboom D., Macdonald D., Giannini C., Suh J.H., et al. Phase II trial of preirradiation and concurrent temozolomide in patients with newly diagnosed anaplastic oligodendrogliomas and mixed anaplastic oligoastrocytomas: RTOG BR0131. Neuro-Oncology 2009, 11:167-175.
10. Gan H.K., Rosenthal M.A., Dowling A., Kalnins R., Algar E., Wong N., et al. A phase II trial of primary temozolomide in patients with grade III oligodendroglial brain tumors. Neuro-Oncology 2010, 12:500-507.
11. Bauman G., Fisher B., Watling C., Cairncross J.G., Macdonald D. Adult supratentorial low-grade glioma: long-term experience at a single institution. Int. J. Radiat. Oncol. Biol. Phys. 2009, 75:1401-1407.
12. Tabatabai G., Stupp R., van den Bent M.J., Hegi M.E., Tonn J.C., Wick W., et al. Molecular diagnostics of gliomas: the clinical perspective. Acta Neuropathol. 2010, 120:585-592.
13. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J., et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New Engl. J. Med. 2005, 352:987-996.
14. Hegi M.E., Diserens A.C., Gorlia T., Hamou M.F., de Tribolet N., Weller M., et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. New Engl. J. Med. 2005, 352:997-1003.
15. Cancer Genome Atlas Research Network, Comprehensive genomic characterization defines human glioblastoma genes and core pathways, Nature 455 (2008) 1061-1068.
16. Yan H., Parsons D.W., Jin G., McLendon R., Rasheed B.A., Yuan W., et al. IDH1 and IDH2 mutations in gliomas. New Engl. J. Med. 2009, 360:765-773.
17. Weller M., Felsberg J., Hartmann C., Berger H., Steinbach J.P., Schramm J., et al. Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: a prospective translational study of the German Glioma Network. J. Clin. Oncol. 2009, 27:5743-5750.
18. Zhao S., Lin Y., Xu W., Jiang W., Zha Z., Wang P., et al. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science 2009, 324:261-265.
19. Dang L., White D.W., Gross S., Bennett B.D., Bittinger M.A., Driggers E.M., et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009, 462:739-744.
20. Kruse J.P., Gu W. Modes of p53 regulation. Cell 2009, 137:609-622.
21. Farnebo M., Bykov V.J., Wiman K.G. The p53 tumor suppressor: a master regulator of diverse cellular processes and therapeutic target in cancer. Biochem. Biophys. Res. Commun. 2010, 396:85-89.
22. Green D.R., Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009, 458:1127-1130.
23. Ohgaki H., Dessen P., Jourde B., Horstmann S., Nishikawa T., Di Patre P.L., et al. Genetic pathways to glioblastoma: a population-based study. Cancer Res. 2004, 64:6892-6899.
24. Lang F.F., Bruner J.M., Fuller G.N., Aldape K., Prados M.D., Chang S., et al. Phase I trial of adenovirus-mediated p53 gene therapy for recurrent glioma: biological and clinical results. J. Clin. Oncol. 2003, 21:2508-2518.
25. Foster B.A., Coffey H.A., Morin M.J., Rastinejad F. Pharmacological rescue of mutant p53 conformation and function. Science 1999, 286:2507-2510.
26. Wischhusen J., Naumann U., Ohgaki H., Rastinejad F., Weller M. CP-31398, a novel p53-stabilizing agent, induces p53-dependent and p53-independent glioma cell death. Oncogene 2003, 22:8233-8245.
27. Bykov V.J., Issaeva N., Zache N., Shilov A., Hultcrantz M., Bergman J., et al. Reactivation of mutant p53 and induction of apoptosis in human tumor cells by maleimide analogs. J. Biol. Chem. 2005, 280:30384-30391.
28. Bykov V.J., Issaeva N., Shilov A., Hultcrantz M., Pugacheva E., Chumakov P., et al. Restoration of the tumor suppressor function to mutant p53 by a low-molecular-weight compound. Nat. Med. 2002, 8:282-288.
29. Weinmann L., Wischhusen J., Demma M.J., Naumann U., Roth P., Dasmahapatra B., et al. A novel p53 rescue compound induces p53-dependent growth arrest and sensitises glioma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ. 2008, 15:718-729.
30. Vassilev L.T. Small-molecule antagonists of p53-MDM2 binding: research tools and potential therapeutics. Cell Cycle 2004, 3:419-421.
31. Shangary S., Qin D., McEachern D., Liu M., Miller R.S., Qiu S., et al. Temporal activation of p53 by a specific MDM2 inhibitor is selectively toxic to tumors and leads to complete tumor growth inhibition. Proc. Natl. Acad. Sci. USA 2008, 105:3933-3938.
32. Merkel C.A., da Silva Soares R.B., de Carvalho A.C., Zanatta D.B., Bajgelman M.C., Fratini P., et al. Activation of endogenous p53 by combined p19Arf gene transfer and nutlin-3 drug treatment modalities in the murine cell lines B16 and C6. BMC Cancer 2010, 10:316.
33. Jackson M.W., Lindstrom M.S., Berberich S.J. MdmX binding to ARF affects Mdm2 protein stability and p53 transactivation. J. Biol. Chem. 2001, 276:25336-25341.
34. Hu B., Gilkes D.M., Farooqi B., Sebti S.M., Chen J. MDMX overexpression prevents p53 activation by the MDM2 inhibitor Nutlin. J. Biol. Chem. 2006, 281:33030-33035.
35. Liu M., Li C., Pazgier M., Li C., Mao Y., Lv Y., et al. D-peptide inhibitors of the p53-MDM2 interaction for targeted molecular therapy of malignant neoplasms. Proc. Natl. Acad. Sci. USA 2010, 107:14321-14326.
36. Krajewski S., Krajewska M., Ehrmann J., Sikorska M., Lach B., Chatten J., et al. Immunohistochemical analysis of Bcl-2, Bcl-X, Mcl-1, and Bax in tumors of central and peripheral nervous system origin. Am. J. Pathol. 1997, 150:805-814.
37. McDonald F.E., Ironside J.W., Gregor A., Wyatt B., Stewart M., Rye R., et al. The prognostic influence of bcl-2 in malignant glioma. Br. J. Cancer 2002, 86:1899-1904.
38. Jiang Z., Zheng X., Rich K.M. Down-regulation of Bcl-2 and Bcl-xL expression with bispecific antisense treatment in glioblastoma cell lines induce cell death. J. Neurochem. 2003, 84:273-281.
39. Zhu C.J., Li Y.B., Wong M.C. Expression of antisense bcl-2 cDNA abolishes tumorigenicity and enhances chemosensitivity of human malignant glioma cells. J. Neurosci. Res. 2003, 74:60-66.
40. Naumann U., Schmidt F., Wick W., Frank B., Weit S., Gillissen B., et al. Adenoviral natural born killer gene therapy for malignant glioma. Human. Gene Ther. 2003, 14:1235-1246.
41. Vogler M., Weber K., Dinsdale D., Schmitz I., Schulze-Osthoff K., Dyer M.J., et al. Different forms of cell death induced by putative BCL2 inhibitors. Cell Death Differ. 2009, 16:1030-1039.
42. Voss V., Senft C., Lang V., Ronellenfitsch M.W., Steinbach J.P., Seifert V., et al. The pan-Bcl-2 inhibitor (-)-gossypol triggers autophagic cell death in malignant glioma. Mol. Cancer Res. 2010, 8:1002-1016.
43. van Delft M.F., Wei A.H., Mason K.D., Vandenberg C.J., Chen L., Czabotar P.E., et al. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell. 2006, 10:389-399.
44. Tagscherer K.E., Fassl A., Campos B., Farhadi M., Kraemer A., Bock B.C., et al. A novel small molecule inhibitor of Bcl-2 family proteins. Oncogene 2008, 27:6646-6656.
45. Chan J.A., Krichevsky A.M., Kosik K.S. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005, 65:6029-6033.
46. Xu J., Liao X., Wong C. Downregulations of B-cell lymphoma 2 and myeloid cell leukemia sequence 1 by microRNA 153 induce apoptosis in a glioblastoma cell line DBTRG-05MG. Int. J. Cancer 2010, 126:1029-1035.
47. Shi L., Chen J., Yang J., Pan T., Zhang S., Wang Z. MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax/Bcl-2 ratio and caspase-3 activity. Brain Res. 2010, 1352:255-264.
48. Gyrd-Hansen M., Meier P. IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat. Rev. Cancer. 2010, 10:561-574.
49. Wagenknecht B., Glaser T., Naumann U., Kugler S., Isenmann S., Bahr M., et al. Expression and biological activity of X-linked inhibitor of apoptosis (XIAP) in human malignant glioma. Cell Death Differ. 1999, 6:370-376.
50. Du C., Fang M., Li Y., Li L., Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000, 102:33-42.
51. Fulda S., Wick W., Weller M., Debatin K.M. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 2002, 8:808-815.
52. Giagkousiklidis S., Vogler M., Westhoff M.A., Kasperczyk H., Debatin K.M., Fulda S. Sensitization for gamma-irradiation-induced apoptosis by second mitochondria-derived activator of caspase. Cancer Res. 2005, 65:10502-10513.
53. Li L., Thomas R.M., Suzuki H., De Brabander J.K., Wang X., Harran P.G. A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death. Science 2004, 305:1471-1474.
54. Flygare J.A., Fairbrother W.J. Small-molecule pan-IAP antagonists: a patent review. Expert Opin. Ther. Pat. 2010, 20:251-267.
55. Ohgaki H., Kleihues P. Genetic alterations and signaling pathways in the evolution of gliomas. Cancer Sci. 2009, 100:2235-2241.
56. Frederick L., Wang X.Y., Eley G., James C.D. Diversity and frequency of epidermal growth factor receptor mutations in human glioblastomas. Cancer Res. 2000, 60:1383-1387.
57. Kleihues P., Ohgaki H. Primary and secondary glioblastomas: from concept to clinical diagnosis. Neuro-Oncology 1999, 1:44-51.
58. Reardon D.A., Desjardins A., Vredenburgh J.J., Gururangan S., Friedman A.H., Herndon J.E., et al. Phase 2 trial of erlotinib plus sirolimus in adults with recurrent glioblastoma. J. Neurooncol. 2010, 96:219-230.
59. de Groot J.F., Gilbert M.R., Aldape K., Hess K.R., Hanna T.A., Ictech S., et al. Phase II study of carboplatin and erlotinib (Tarceva, OSI-774) in patients with recurrent glioblastoma. J. Neurooncol. 2008, 90:89-97.
60. Prados M.D., Chang S.M., Butowski N., DeBoer R., Parvataneni R., Carliner H., et al. Phase II study of erlotinib plus temozolomide during and after radiation therapy in patients with newly diagnosed glioblastoma multiforme or gliosarcoma. J. Clin. Oncol. 2009, 27:579-584.
61. van den Bent M.J., Brandes A.A., Rampling R., Kouwenhoven M.C., Kros J.M., Carpentier A.F., et al. Randomized phase II trial of erlotinib versus temozolomide or carmustine in recurrent glioblastoma: EORTC brain tumor group study 26034. J. Clin. Oncol. 2009, 27:1268-1274.
62. Mellinghoff I.K., Wang M.Y., Vivanco I., Haas-Kogan D.A., Zhu S., Dia E.Q., et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. New Engl. J. Med. 2005, 353:2012-2024.
63. Raymond E., Brandes A.A., Dittrich C., Fumoleau P., Coudert B., Clement P.M., et al. Phase II study of imatinib in patients with recurrent gliomas of various histologies: a European Organisation for Research and Treatment of Cancer Brain Tumor Group Study. J. Clin. Oncol. 2008, 26:4659-4665.
64. Dresemann G., Weller M., Rosenthal M.A., Wedding U., Wagner W., Engel E., et al. Imatinib in combination with hydroxyurea versus hydroxyurea alone as oral therapy in patients with progressive pretreated glioblastoma resistant to standard dose temozolomide. J. Neurooncol. 2010, 96:393-402.
65. 2-terminal kinase pathways. Mol. Cancer Ther. 2006, 5:2378-2387.
66. Jane E.P., Premkumar D.R., Pollack I.F. Coadministration of sorafenib with rottlerin potently inhibits cell proliferation and migration in human malignant glioma cells. J. Pharmacol. Exp. Ther. 2006, 319:1070-1080.
67. Hainsworth J.D., Ervin T., Friedman E., Priego V., Murphy P.B., Clark B.L., et al. Concurrent radiotherapy and temozolomide followed by temozolomide and sorafenib in the first-line treatment of patients with glioblastoma multiforme. Cancer 2010, 116:3663-3669.
68. Galanis E., Buckner J.C., Maurer M.J., Kreisberg J.I., Ballman K., Boni J., et al. Phase II trial of temsirolimus (CCI-779) in recurrent glioblastoma multiforme: a North Central Cancer Treatment Group Study. J. Clin. Oncol. 2005, 23:5294-5304.
69. Wang M.Y., Lu K.V., Zhu S., Dia E.Q., Vivanco I., Shackleford G.M., et al. Mammalian target of rapamycin inhibition promotes response to epidermal growth factor receptor kinase inhibitors in PTEN-deficient and PTEN-intact glioblastoma cells. Cancer Res. 2006, 66:7864-7869.
70. Trauth B.C., Klas C., Peters A.M., Matzku S., Moller P., Falk W., et al. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 1989, 245:301-305.
71. Yonehara S., Ishii A., Yonehara M. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J. Exp. Med. 1989, 169:1747-1756.
72. Oehm A., Behrmann I., Falk W., Pawlita M., Maier G., Klas C., et al. J. Biol. Chem. 1992, 267:10709-10715.
73. Suda T., Takahashi T., Golstein P., Nagata S. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 1993, 75:1169-1178.
74. Weller M., Frei K., Groscurth P., Krammer P.H., Yonekawa Y., Fontana A. Anti-Fas/APO-1 antibody-mediated apoptosis of cultured human glioma cells. Induction and modulation of sensitivity by cytokines. J. Clin. Invest. 1994, 94:954-964.
75. Roth W., Fontana A., Trepel M., Reed J.C., Dichgans J., Weller M. Immunochemotherapy of malignant glioma: synergistic activity of CD95 ligand and chemotherapeutics. Cancer Immunol. Immunother. 1997, 44:55-63.
76. Holler N., Tardivel A., Kovacsovics-Bankowski M., Hertig S., Gaide O., Martinon F., et al. Two adjacent trimeric Fas ligands are required for Fas signaling and formation of a death-inducing signaling complex. Mol. Cell Biol. 2003, 23:1428-1440.
77. G. Eisele, P. Roth, K. Hasenbach, S. Aulwurm, F. Wolpert, G. Tabatabai, W. Wick, M. Weller, APO010, a synthetic hexameric (CD95) ligand, induces human glioma cell death in vitro and in vivo. Neuro-Oncology (2010), doi:10.1093/neuonc/noq176.
78. Rensing-Ehl A., Frei K., Flury R., Matiba B., Mariani S.M., Weller M., et al. Local Fas/APO-1 (CD95) ligand-mediated tumor cell killing in vivo. Eur. J. Immunol. 1995, 25:2253-2258.
79. Ogasawara J., Watanabe-Fukunaga R., Adachi M., Matsuzawa A., Kasugai T., Kitamura Y., et al. Lethal effect of the anti-Fas antibody in mice. Nature 1993, 364:806-809.
80. Felderhoff-Mueser U., Taylor D.L., Greenwood K., Kozma M., Stibenz D., Joashi U.C., et al. Fas/CD95/APO-1 can function as a death receptor for neuronal cells in vitro and in vivo and is upregulated following cerebral hypoxic-ischemic injury to the developing rat brain. Brain Pathol. 2000, 10:17-29.
81. Lautrette C., Giraud S., Vermot-Desroches C., Preud'homme J.L., Jauberteau M.O. Expression of a functional Fas death receptor by human foetal motoneurons. Neuroscience 2003, 119:377-385.
82. Raoul C., Henderson C.E., Pettmann B. Programmed cell death of embryonic motoneurons triggered through the Fas death receptor. J. Cell Biol. 1999, 147:1049-1062.
83. Beier C.P., Wischhusen J., Gleichmann M., Gerhardt E., Pekanovic A., Krueger A., et al. FasL (CD95L/APO-1L) resistance of neurons mediated by phosphatidylinositol 3-kinase-Akt/protein kinase B-dependent expression of lifeguard/neuronal membrane protein 35. J. Neurosci. 2005, 25:6765-6774.
84. Kleber S., Sancho-Martinez I., Wiestler B., Beisel A., Gieffers C., Hill O., et al. Yes and PI3K bind CD95 to signal invasion of glioblastoma. Cancer Cell. 2008, 13:235-248.
85. Chen L., Park S.M., Tumanov A.V., Hau A., Sawada K., Feig C., et al. CD95 promotes tumour growth. Nature 2010, 465:492-496.
86. Ashkenazi A., Pai R.C., Fong S., Leung S., Lawrence D.A., Marsters S.A., et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 1999, 104:155-162.
87. Naumann U., Wick W., Beschorner R., Meyermann R., Weller M. Expression and functional activity of osteoprotegerin in human malignant gliomas. Acta Neuropathol. 2004, 107:17-22.
88. Zauli G., Melloni E., Capitani S., Secchiero P. Role of full-length osteoprotegerin in tumor cell biology. Cell Mol. Life Sci. 2009, 66:841-851.
89. Rieger J., Naumann U., Glaser T., Ashkenazi A., Weller M. APO2 ligand: a novel lethal weapon against malignant glioma?. FEBS Lett. 1998, 427:124-128.
90. Frank S., Kohler U., Schackert G., Schackert H.K. Expression of TRAIL and its receptors in human brain tumors. Biochem. Biophys. Res. Commun. 1999, 257:454-459.
91. Kuijlen J.M., Mooij J.J., Platteel I., Hoving E.W., van der Graaf W.T., Span M.M., et al. TRAIL-receptor expression is an independent prognostic factor for survival in patients with a primary glioblastoma multiforme. J. Neurooncol. 2006, 78:161-171.
92. Grund K., Ahmadi R., Jung F., Funke V., Gdynia G., Benner A., et al. Troglitazone-mediated sensitization to TRAIL-induced apoptosis is regulated by proteasome-dependent degradation of FLIP and ERK1/2-dependent phosphorylation of BAD. Cancer Biol. Ther. 2008, 7:1982-1990.
93. Dorr J., Bechmann I., Waiczies S., Aktas O., Walczak H., Krammer P.H., et al. Lack of tumor necrosis factor-related apoptosis-inducing ligand but presence of its receptors in the human brain. J. Neurosci. 2002, 22:1-5. RC209.
94. Nitsch R., Bechmann I., Deisz R.A., Haas D., Lehmann T.N., Wendling U., et al. Human brain-cell death induced by tumour-necrosis-factor-related apoptosis-inducing ligand (TRAIL). Lancet 2000, 356:827-828.
95. Lawrence D., Shahrokh Z., Marsters S., Achilles K., Shih D., Mounho B., et al. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat. Med. 2001, 7:383-385.
96. Kelley R.F., Totpal K., Lindstrom S.H., Mathieu M., Billeci K., Deforge L., et al. Receptor-selective mutants of apoptosis-inducing ligand 2/tumor necrosis factor-related apoptosis-inducing ligand reveal a greater contribution of death receptor (DR) 5 than DR4 to apoptosis signaling. J. Biol. Chem. 2005, 280:2205-2212.
97. Jeong M., Kwon Y.S., Park S.H., Kim C.Y., Jeun S.S., Song K.W., et al. Possible novel therapy for malignant gliomas with secretable trimeric TRAIL. PLoS One 2009, 4:e4545.
98. M. Nagane, S. Shimizu, E. Mori, S. Kataoka, Y. Shiokawa, Predominant antitumor effects by fully human anti-TRAIL-receptor2 (DR5) monoclonal antibodies in human glioma cells in vitro and in vivo, Neuro-Oncology (2010) (epub ahead of print).
99. Rieger J., Frank B., Weller M., Wick W. Mechanisms of resistance of human glioma cells to Apo2 ligand/TNF-related apoptosis-inducing ligand. Cell Physiol. Biochem. 2007, 20:23-34.
100. Rohn T.A., Wagenknecht B., Roth W., Naumann U., Gulbins E., Krammer P.H., et al. CCNU-dependent potentiation of TRAIL/Apo2L-induced apoptosis in human glioma cells is p53-independent but may involve enhanced cytochrome c release. Oncogene 2001, 20:4128-4137.
101. Fiveash J.B., Gillespie G.Y., Oliver P.G., Zhou T., Belenky M.L., Buchsbaum D.J. Enhancement of glioma radiotherapy and chemotherapy response with targeted antibody therapy against death receptor 5. Int. J. Radiat. Oncol. Biol. Phys. 2008, 71:507-516.
102. Nagane M., Pan G., Weddle J.J., Dixit V.M., Cavenee W.K., Huang H.J. Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res. 2000, 60:847-853.
103. Saito R., Bringas J.R., Panner A., Tamas M., Pieper R.O., Berger M.S., et al. Convection-enhanced delivery of tumor necrosis factor-related apoptosis-inducing ligand with systemic administration of temozolomide prolongs survival in an intracranial glioblastoma xenograft model. Cancer Res. 2004, 64:6858-6862.
104. Verbrugge I., deVries E., Tait S.W., Wissink E.H., Walczak H., Verheij M., et al. Ionizing radiation modulates the TRAIL death-inducing signaling complex, allowing bypass of the mitochondrial apoptosis pathway. Oncogene 2008, 27:574-584.
105. Nagane M., Cavenee W.K., Shiokawa Y. Synergistic cytotoxicity through the activation of multiple apoptosis pathways in human glioma cells induced by combined treatment with ionizing radiation and tumor necrosis factor-related apoptosis-inducing ligand. J. Neurosurg. 2007, 106:407-416.
106. Roth P., Kissel M., Herrmann C., Eisele G., Leban J., Weller M., et al. SC68896, a novel small molecule proteasome inhibitor, exerts antiglioma activity in vitro and in vivo. Clin. Cancer Res. 2009, 15:6609-6618.
107. Opel D., Westhoff M.A., Bender A., Braun V., Debatin K.M., Fulda S. Phosphatidylinositol 3-kinase inhibition broadly sensitizes glioblastoma cells to death receptor- and drug-induced apoptosis. Cancer Res. 2008, 68:6271-6280.
108. Hetschko H., Voss V., Horn S., Seifert V., Prehn J.H., Kogel D. Pharmacological inhibition of Bcl-2 family members reactivates TRAIL-induced apoptosis in malignant glioma. J. Neurooncol. 2008, 86:265-272.
109. Corsten M.F., Miranda R., Kasmieh R., Krichevsky A.M., Weissleder R., Shah K. MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res. 2007, 67:8994-9000.
110. Schultze K., Bock B., Eckert A., Oevermann L., Ramacher D., Wiestler O., et al. Troglitazone sensitizes tumor cells to TRAIL-induced apoptosis via down-regulation of FLIP and Survivin. Apoptosis 2006, 11:1503-1512.
111. Nakasu S., Nakasu Y., Nioka H., Nakajima M., Handa J. Bcl-2 protein expression in tumors of the central nervous system. Acta Neuropathol. 1994, 88:520-526.
112. Ellison D.W., Steart P.V., Gatter K.C., Weller R.O. Apoptosis in cerebral astrocytic tumours and its relationship to expression of the bcl-2 and p53 proteins. Neuropathol. Appl. Neurobiol. 1995, 21:352-361.
113. Schiffer D., Cavalla P., Migheli A., Giordana M.T., Chiado-Piat L. Bcl-2 distribution in neuroepithelial tumors: an immunohistochemical study. J. Neurooncol. 1996, 27:101-109.
114. D.T. Yew, H.H. Wang, D.R. Zheng, Apoptosis in astrocytomas with different grades of malignancy, Acta Neurochir. (Wien) 140 (1998) 341-347.
115. Frankel B., Longo S.L., Ryken T.C. Human astrocytomas co-expressing Fas and Fas ligand also produce TGFbeta2 and Bcl-2. J. Neurooncol. 1999, 44:205-212.
116. Fels C., Schafer C., Huppe B., Bahn H., Heidecke V., Kramm C.M., et al. Bcl-2 expression in higher-grade human glioma: a clinical and experimental study. J. Neurooncol. 2000, 48:207-216.
117. Angileri F.F., Aguennouz M., Conti A., La Torre D., Cardali S., Crupi R., et al. Nuclear factor-kappaB activation and differential expression of survivin and Bcl-2 in human grade 2-4 astrocytomas. Cancer 2008, 112:2258-2266.
118. Krishna M., Smith T.W., Recht L.D. Expression of bcl-2 in reactive and neoplastic astrocytes: lack of correlation with presence or degree of malignancy. J. Neurosurg. 1995, 83:1017-1022.
119. R.S. Carroll, J. Zhang, B.W. Chauncey, K. Chantziara, M.P. Frosch, P.M. Black, Apoptosis in astrocytic neoplasms, Acta Neurochir. (Wien) 139 (1997) 845-850.
120. Newcomb E.W., Bhalla S.K., Parrish C.L., Hayes R.L., Cohen H., Miller D.C. Bcl-2 protein expression in astrocytomas in relation to patient survival and p53 gene status. Acta Neuropathol. 1997, 94:369-375.
121. Rodriguez-Pereira C., Suarez-Penaranda J.M., Barros F., Sobrido M.J., Vazquez-Salvado M., Forteza J. Analysis of 2 antiapoptotic factors in gliomas: bcl-2 overexpression and p53 mutations. Arch. Pathol. Lab. Med. 2001, 125:218-223.
122. Kajiwara Y., Yamasaki F., Hama S., Yahara K., Yoshioka H., Sugiyama K., et al. Expression of survivin in astrocytic tumors: correlation with malignant grade and prognosis. Cancer 2003, 97:1077-1083.
123. Martin S., Toquet C., Oliver L., Cartron P.F., Perrin P., Meflah K., et al. Expression of bcl-2, bax and bcl-xl in human gliomas: a re-appraisal. J. Neurooncol. 2001, 52:129-139.
124. Rieger L., Weller M., Bornemann A., Schabet M., Dichgans J., Meyermann R. BCL-2 family protein expression in human malignant glioma: a clinical-pathological correlative study. J. Neurol. Sci. 1998, 155:68-75.
125. Strik H., Deininger M., Streffer J., Grote E., Wickboldt J., Dichgans J., et al. BCL-2 family protein expression in initial and recurrent glioblastomas: modulation by radiochemotherapy. J. Neurol. Neurosurg. Psychiatry 1999, 67:763-768.
126. Sasaki T., Lopes M.B., Hankins G.R., Helm G.A. Expression of survivin, an inhibitor of apoptosis protein, in tumors of the nervous system. Acta Neuropathol. 2002, 104:105-109.
127. Das A., Tan W.L., Teo J., Smith D.R. Expression of survivin in primary glioblastomas. J. Cancer Res. Clin. Oncol. 2002, 128:302-306.
128. Chakravarti A., Noll E., Black P.M., Finkelstein D.F., Finkelstein D.M., Dyson N.J., et al. Quantitatively determined survivin expression levels are of prognostic value in human gliomas. J. Clin. Oncol. 2002, 20:1063-1068.
129. Uematsu M., Ohsawa I., Aokage T., Nishimaki K., Matsumoto K., Takahashi H., et al. Prognostic significance of the immunohistochemical index of survivin in glioma: a comparative study with the MIB-1 index. J. Neurooncol. 2005, 72:231-238.
130. Zhen H.N., Zhang X., Hu P.Z., Yang T.T., Fei Z., Zhang J.N., et al. Survivin expression and its relation with proliferation, apoptosis, and angiogenesis in brain gliomas. Cancer 2005, 104:2775-2783.
131. Preusser M., Gelpi E., Matej R., Marosi C., Dieckmann K., Rossler K., et al. No prognostic impact of survivin expression in glioblastoma. Acta Neuropathol. 2005, 109:534-538.
132. Liu X., Chen N., Wang X., He Y., Chen X., Huang Y., et al. Apoptosis and proliferation markers in diffusely infiltrating astrocytomas: profiling of 17 molecules. J. Neuropathol. Exp. Neurol. 2006, 65:905-913.
133. Saito T., Arifin M.T., Hama S., Kajiwara Y., Sugiyama K., Yamasaki F., et al. Survivin subcellular localization in high-grade astrocytomas: simultaneous expression in both nucleus and cytoplasm is negative prognostic marker. J. Neurooncol. 2007, 82:193-198.
134. Kogiku M., Ohsawa I., Matsumoto K., Sugisaki Y., Takahashi H., Teramoto A., et al. Prognosis of glioma patients by combined immunostaining for survivin, Ki-67 and epidermal growth factor receptor. J. Clin. Neurosci. 2008, 15:1198-1203.
135. Shirai K., Suzuki Y., Oka K., Noda S.E., Katoh H., Suzuki Y., et al. Nuclear survivin expression predicts poorer prognosis in glioblastoma. J. Neurooncol. 2009, 91:353-358.
136. Tachibana O., Nakazawa H., Lampe J., Watanabe K., Kleihues P., Ohgaki H. Expression of Fas/APO-1 during the progression of astrocytomas. Cancer Res. 1995, 55:5528-5530.
137. Gratas C., Tohma Y., Van Meir E.G., Klein M., Tenan M., Ishii N., et al. Fas ligand expression in glioblastoma cell lines and primary astrocytic brain tumors. Brain Pathol. 1997, 7:863-869.
138. Saas P., Walker P.R., Hahne M., Quiquerez A.L., Schnuriger V., Perrin G., et al. Fas ligand expression by astrocytoma in vivo: maintaining immune privilege in the brain?. J. Clin. Invest. 1997, 99:1173-1178.
139. Husain N., Chiocca E.A., Rainov N., Louis D.N., Zervas N.T. Co-expression of Fas and Fas ligand in malignant glial tumors and cell lines. Acta Neuropathol. 1998, 95:287-290.
140. Frankel B., Longo S.L., Leach C., Canute G.W., Ryken T.C. Apoptosis and survival in high-grade astrocytomas as related to tumor Fas (APO-1/CD95) expression. J. Neurooncol. 2002, 59:27-34.
141. Strege R.J., Godt C., Stark A.M., Hugo H.H., Mehdorn H.M. Protein expression of Fas, Fas ligand, Bcl-2 and TGFbeta2 and correlation with survival in initial and recurrent human gliomas. J. Neurooncol. 2004, 67:29-39.
142. Rieger J., Ohgaki H., Kleihues P., Weller M. Human astrocytic brain tumors express AP02L/TRAIL. Acta Neuropathol. 1999, 97:1-4.
143. Bodey B., Bodey V., Siegel S.E., Nasir A., Coppola D., Hakam A., et al. Immunocytochemical detection of members of the caspase cascade of apoptosis in high-grade astrocytomas. In Vivo 2004, 18:593-602.
144. Ashley D.M., Riffkin C.D., Muscat A.M., Knight M.J., Kaye A.H., Novak U., et al. Caspase 8 is absent or low in many ex vivo gliomas. Cancer 2005, 104:1487-1496.
145. Conti A., Ageunnouz M., La Torre D., Cardali S., Angileri F.F., Buemi C., et al. Expression of the tumor necrosis factor receptor-associated factors 1 and 2 and regulation of the nuclear factor-kappaB antiapoptotic activity in human gliomas. J. Neurosurg. 2005, 103:873-881.
146. Kobayashi T., Masumoto J., Tada T., Nomiyama T., Hongo K., Nakayama J. Prognostic significance of the immunohistochemical staining of cleaved caspase-3, an activated form of caspase-3, in gliomas. Clin. Cancer Res. 2007, 13:3868-3874.
147. Tirapelli L.F., Bolini P.H., Tirapelli D.P., Peria F.M., Becker A.N., Saggioro F.P., et al. Caspase-3 and Bcl-2 expression in glioblastoma: an immunohistochemical study. Arq. Neuropsiquiatria 2010, 68:603-607.