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

Journal of Neurosurgery

Volumn 106, Issue 3, 2007, Pages 407-416

  Nagane, Motoo ^a   Cavenee, Webster K ^b,c   Shiokawa, Yoshiaki ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis tumor necrosis factor related apoptosis inducing ligand; DR5; Glioblastoma multiforme; Radiotherapy

Indexed keywords

APOPTOSOME; CASPASE 3; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; CYTOCHROME C; CYTOKINE RESPONSE MODIFIER A; DEATH RECEPTOR 5; FAS ASSOCIATED DEATH DOMAIN PROTEIN; PROTEIN BCL X; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; ASTROCYTE; CELL DEATH; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; GENOTOXICITY; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IONIZING RADIATION; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

APOPTOSIS; CASPASES; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; GLIOMA; HUMANS; RADIATION, IONIZING; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 33847609303     PISSN: 00223085     EISSN: 00223085     Source Type: Journal    
DOI: 10.3171/jns.2007.106.3.407     Document Type: Article

References (66)

1. Almasan A, Ashkenazi A: Apo2L/TRAIL: apoptosis signaling, biology, and potential for cancer therapy. Cytokine Growth Factor Rev 14:337-348, 2003
2. Ashkenazi A: Targeting death and decoy receptors of the tumornecrosis factor superfamily. Nat Rev Cancer 2:420-430, 2002
3. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, et al: Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104:155-162, 1999
4. Chinnaiyan AM, Prasad U, Shankar S, Hamstra DA, Shanaiah M, Chenevert TL, et al: Combined effect of tumor necrosis factor-related apoptosis-inducing ligand and ionizing radiation in breast cancer therapy. Proc Natl Acad Sci U S A 97:1754-1759, 2000
5. Chou TC, Talalay P: Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22:27-55, 1984
6. The Committee of Brain Tumor Registry of Japan: Report of Brain Tumor Registry of Japan (1969-1996). Neurol Med Chir (Tokyo) 43 Suppl, 2003
7. Danial NN, Korsmeyer SJ: Cell death: critical control points. Cell 116:205-219, 2004
8. Degli-Esposti MA, Dougall WC, Smolak PJ, Waugh JY, Smith CA, Goodwin RG: The novel receptor TRAIL-R4 induces NFkappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity 7:813-820, 1997
9. Ekert PG, Silke J, Vaux DL: Caspase inhibitors. Cell Death Differ 6:1081-1086, 1999
10. Emery JG, McDonnell P, Burke MB, Deen KC, Lyn S, Silverman C, et al: Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J Biol Chem 273:14363-14367, 1998
11. Frank S, Köhler U, Schackert G, Schackert HK: Expression of TRAIL and its receptors in human brain tumors. Biochem Biophys Res Commun 257:454-459, 1999
12. Furnari FB, Lin H, Huang HS, Cavenee WK: Growth suppression of glioma cells by PTEN requires a functional phosphatase catalytic domain. Proc Natl Acad Sci U S A 94:12479-12484, 1997
13. Gong B, Almasan A: Apo2 ligand/TNF-related apoptosis-inducing ligand and death receptor 5 mediate the apoptotic signaling induced by ionizing radiation in leukemic cells. Cancer Res 60: 5754-5760, 2000
14. Green DR, Reed JC: Mitochondria and apoptosis. Science 281: 1309-1312, 1998
15. Guchelaar HJ, Vermes A, Vermes I, Haanen C: Apoptosis: molecular mechanisms and implications for cancer chemotherapy. Pharm World Sci 19:119-125, 1997
16. Havell EA, Fiers W, North RJ: The antitumor function of tumor necrosis factor (TNF), I. Therapeutic action of TNF against an established murine sarcoma is indirect, immunologically dependent, and limited by severe toxicity. J Exp Med 167:1067-1085, 1988
17. Ichikawa K, Liu W, Zhao L, Wang Z, Liu D, Ohtsuka T, et al: Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat Med 7:954-960, 2001
18. Jelsma R, Bucy PC: The treatment of glioblastoma multiforme of the brain. J Neurosurg 27:388-400, 1967
19. Jo M, Kim TH, Seol DW, Esplen JE, Dorko K, Billiar TR, et al: Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat Med 6:564-567, 2000
20. Kaufmann SH, Earnshaw WC: Induction of apoptosis by cancer chemotherapy. Exp Cell Res 256:42-49, 2000
21. Kondziolka D, Flickinger JC, Bissonette DJ, Bozik M, Lunsford LD: Survival benefit of stereotactic radiosurgery for patients with malignant glial neoplasms. Neurosurgery 41:776-785, 1997
22. Kristiansen K, Hagen S, Kollevold T, Torvik A, Holme I, Nesbakken R, et al: Combined modality therapy of operated astrocytomas grade III and IV. Confirmation of the value of postoperative irradiation and lack of potentiation of bleomycin on survival time: a prospective multicenter trial of the Scandinavian Glioblastoma Study Group. Cancer 47:649-652, 1981
23. Kuwana T, Newmeyer DD: Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15:691-699, 2003
24. Lawrence D, Shahrokh Z, Marsters S, Achilles K, Shih D, Mounho B, et al: Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat Med 7:383-385, 2001
25. Leverkus M, Neumann M, Mengling T, Rauch CT, Brocker EB, Krammer PH, et al: Regulation of tumor necrosis factor-related apoptosis-inducing ligand sensitivity in primary and transformed human keratinocytes. Cancer Res 60:553-559, 2000
26. Levin VA, Silver P, Hannigan J, Wara WM, Gutin PH, Davis RL, et al: Superiority of post-radiotherapy adjuvant chemotherapy with CCNU, procarbazine, and vincristine (PCV) over BCNU for anaplastic gliomas: NCOG 6G61 final report. Int J Radiat Oncol Biol Phys 18:321-324, 1990
27. Lorenzo HK, Susin SA: Mitochondrial effectors in caspase-independent cell death. FEBS Lett 557:14-20, 2004
28. Marini P, Jendrossek V, Durand E, Gruber C, Budach W, Belka C: Molecular requirements for the combined effects of TRAIL and ionising radiation. Radiother Oncol 68:189-198, 2003
29. Marsters SA, Sheridan JP, Pitti RM, Huang A, Skubatch M, Baldwin D, et al: A novel receptor for Apo2L/TRAIL contains a truncated death domain. Curr Biol 7:1003-1006, 1997
30. Mosmann T: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63, 1983
31. Nagane M, Asai A, Shibui S, Nomura K, Kuchino Y: Application of antisense ribonucleic acid complementary to O6-methylguanine-deoxyribonucleic acid methyltransferase messenger ribonucleic acid for therapy of malignant gliomas. Neurosurgery 41: 434-441 1997
32. Nagane M, Coufal F, Lin H, Bögler O, Cavenee WK, Huang HJS: A common mutant epidermal growth factor receptor confers enhanced tumorigenicity on human glioblastoma cells by increasing proliferation and reducing apoptosis. Cancer Res 56:5079-5086, 1996
33. Nagane M, Pan G, Weddle JJ, Dixit VM, Cavenee WK, Huang HJS: 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 60:847-853, 2000
34. Nagata S: Apoptosis by death factor. Cell 88:355-365, 1997
35. 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 364:806-809, 1993
36. Pan G, Ni J, Wei YF, Yu G, Gentz R, Dixit VM: An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 277:815-818, 1997
37. Pan G, O'Rourke K, Chinnaiyan AM, Gentz R, Ebner R, Ni J, et al: The receptor for the cytotoxic ligand TRAIL. Science 276: 111-113, 1997
38. Phillips TL, Levin VA, Ahn DK, Gutin PH, Davis RL, Wilson CB, et al: Evaluation of bromodeoxyuridine in glioblastoma multiforme: a Northern California Cancer Center Phase II study. Int J Radiat Oncol Biol Phys 21:709-714, 1991
39. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A: Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 271: 12687-12690, 1996
40. Qin J, Chaturvedi V, Bonish B, Nickoloff BJ: Avoiding premature apoptosis of normal epidermal cells. Nat Med 7:385-386, 2001
41. Rabin HR, Urtasun RC, Partington J, Koziol D, Sharon M, Walker K: High-dose metronidazole: pharmacokinetics and bioavailability using an iv preparation and application of its use as a radiosensitizer. Cancer Treat Rep 64:1087-1095, 1980
42. Rieger J, Naumann U, Glaser T, Ashkenazi A, Weller M: APO2 ligand: a novel lethal weapon against malignant glioma? FEBS Lett 427:124-128, 1998
43. Rodriguez R, Ritter MA, Fowler JF, Kinsella TJ: Kinetics of cell labeling and thymidine replacement after continuous infusion of halogenated pyrimidines in vivo. Int J Radiat Oncol Biol Phys 29:105-113, 1994
44. Rohn TA, Wagenknecht B, Roth W, Naumann U, Gulbins E, Krammer PH, 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 20:4128-4137, 2001
45. Roth W, Isenmann S, Naumann U, Kugler S, Bahr M, Dichgans J, et al: Locoregional Apo2L/TRAIL eradicates intracranial human malignant glioma xenografts in athymic mice in the absence of neurotoxicity. Biochem Biophys Res Commun 265:479-483, 1999
46. Sarkaria JN, Mehta MP, Loeffler JS, Buatti JM, Chappell RJ, Levin AB, et al: Radiosurgery in the initial management of malignant gliomas: survival comparison with the RTOG recursive partitioning analysis. Radiation Therapy Oncology Group. Int J Radiat Oncol Biol Phys 32:931-941, 1995
47. Shankar S, Singh TR, Srivastava RK: Ionizing radiation enhances the therapeutic potential of TRAIL in prostate cancer in vitro and in vivo: intracellular mechanisms. Prostate 61:35-49, 2004
48. Shankar S, Srivastava RK: Enhancement of therapeutic potential of TRAIL by cancer chemotherapy and irradiation: mechanisms and clinical implications. Drug Resist Updat 7:139-156, 2004
49. Sheikh MS, Burns TF, Huang Y, Wu GS, Amundson S, Brooks KS, et al: p53-dependent and -independent regulation of the death receptor KILLER/DR5 gene expression in response to genotoxic stress and tumor necrosis factor alpha. Cancer Res 58: 1593-1598, 1998
50. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, et al: Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277:818-821, 1997
51. Shrieve DC, Alexander E III, Black PM, Wen PY, Fine HA, Kooy HM, et al: Treatment of patients with primary glioblastoma multiforme with standard postoperative radiotherapy and radiosurgical boost: prognostic factors and long-term outcome. J Neurosurg 90:72-77, 1999
52. Song JH, Song DK, Pyrzynska B, Petruk KC, Van Meir EG, Hao C: TRAIL triggers apoptosis in human malignant glioma cells through extrinsic and intrinsic pathways. Brain Pathol 13: 539-553, 2003
53. Steel G: Combined radiotherapy-chemotherapy: principles, in Steel GG, Adams GE, Horwich E (eds): The Biological Basis of Radiotherapy, ed 2. Amsterdam: Elsevier, 1989, p 267
54. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R: A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 8: 613-621, 2001
55. Tatter SB: Recurrent malignant glioma in adults. Curr Treat Options Oncol 3:509-524, 2002
56. Thornberry NA, Lazebnik Y: Caspases: enemies within. Science 281:1312-1316, 1998
57. Urtasun R, Band P, Chapman JD, Feldstein ML, Mielke B, Fryer C: Radiation and high-dose metronidazole in supratentorial glioblastomas. N Engl J Med 294:1364-1367, 1976
58. Urtasun RC, Cosmatos D, DelRowe J, Kinsella TJ, Lester S, Wasserman T, et al: Iododeoxyuridine (IUdR) combined with radiation in the treatment of malignant glioma: a comparison of short versus long intravenous dose schedules (RTOG 86-12). Int J Radiat Oncol Biol Phys 27:207-214, 1993
59. Van Meir EG, Kikuchi T, Tada M, Li H, Diserens AC, Wojcik BE, et al: Analysis of the p53 gene and its expression in human glioblastoma cells. Cancer Res 54:649-652, 1994
60. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, et al: Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5:157-163, 1999
61. Walker MD, Alexander E Jr, Hunt WE, MacCarty CS, Mahaley MS Jr, Mealey J Jr, et al: Evaluation of BCNU and/or radiotherapy in the treatment of anaplastic gliomas. A cooperative clinical trial. J Neurosurg 49:333-343, 1978
62. Walker MD, Green SB, Byar DP, Alexander E Jr, Batzdorf U, Brooks WH, et al: Randomized comparisons of radiotherapy and nitrosoureas for the treatment of malignant glioma after surgery. N Engl J Med 303:1323-1329, 1980
63. Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, et al: Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3:673-682, 1995
64. Wu GS, Burns TF, McDonald ER III, Jiang W, Meng R, Krantz ID, et al: KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat Genet 17:141-143, 1997
65. Yee JK, Miyanohara A, LaPorte P, Bouic K, Burns JC, Friedmann T: A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. Proc Natl Acad Sci U S A 91:9564-9568, 1994
66. Younes A, Kadin ME: Emerging applications of the tumor necrosis factor family of ligands and receptors in cancer therapy. J Clin Oncol 21:3526-3534, 2003