Apoptosis in glioma cells: Review and analysis of techniques used for study with focus on the laser scanning cytometer

Journal of Neuro-Oncology

Volumn 63, Issue 2, 2003, Pages 129-145

  Amirlak, Bardia ^a,b   Couldwell, William T ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Apoptosis; Flow cytometer; Glioma; Laser scanning cytometer; Programmed cell death

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE; DNA; DNA FRAGMENT; HYPERICIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IRINOTECAN; MARKER; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN P53; STAUROSPORINE;

ACCURACY; APOPTOSIS; BRAIN TUMOR; CELL LEVEL; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CELL PROLIFERATION; CHROMATIN CONDENSATION; CYTOMETRY; CYTOTOXICITY; DNA CLEAVAGE; DNA CONTENT; DNA DENATURATION; DNA STRAND BREAKAGE; ENZYME ACTIVATION; EXPERIMENTATION; FLOW CYTOMETRY; GENE MUTATION; GENE TRANSLOCATION; GLIOMA CELL; HUMAN; INTERMETHOD COMPARISON; LASER SCANNING CYTOMETER; LIGHT SCATTERING; MITOCHONDRIAL MEMBRANE; NONHUMAN; PLOIDY; REVIEW; SOLID TUMOR; TECHNIQUE; TUMOR GROWTH;

APOPTOSIS; BIOLOGICAL MARKERS; BRAIN NEOPLASMS; CELL DIVISION; DNA, NEOPLASM; FLOW CYTOMETRY; GLIOMA; HUMANS; LASERS;

EID: 0038379077     PISSN: 0167594X     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1023906316524     Document Type: Review

References (140)

1. Davis FG et al.: The conditional probability of survival of patients with primary malignant brain tumors: Surveillance, epidemiology, and end results (SEER) data. Cancer, 85: 485-491, 1999
2. Mitchel S, Charles B, Wilson M: In: Berger M (ed) The Gliomas. WB Saunders, New York, 1999, p 796
3. Nieder C, Grosu AL, Molls M: A comparison of treatment results for recurrent malignant gliomas. Cancer Treat Rev 26: 397-409, 2000
4. Shu HK et al.: The intrinsic radioresistance of glioblastoma-derived cell lines is associated with a failure of p53 to induce p21 (BAX) expression. Proc Natl Acad Sci USA 95: 14453-14458, 1998
5. Ekert PG, Vaux DL: Apoptosis, haemopoiesis and leukaemogenesis. Baillieres Clin Haematol 10: 561-576, 1997
6. Vaux DL: Immunopathology of apoptosis - Introduction and overview. Springer Semin Immunopathol 19: 271-278, 1998
7. Vinken PJB, Bruyn GW, Vecht Ch J (eds): Neuro-Oncology Gliomas & Other Primary Tumors of the Brain & Spinal Chord Volume 2. Elsevier Science, 1998, p 614
8. Smith JS, Jenkins RB: Genetic alterations in adult diffuse glioma: Occurrence, significance, and prognostic implications. Front Biosci 5: D213-D231, 2000
9. Kerr JF, Wyllie AH, Currie AR: Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257, 1972
10. Majno G, Joris I: Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146: 3-15, 1995
11. Lockshin RA, Zakeri Z, Tilly JL: When Cells Die: A Comprehensive Evaluation of Apoptosis and Programmed Cell Death. In: Lockshin RA, Zakeri Z, Tilly JL (eds) Wiley-Liss, New York, 1998
12. Saraste A, Pulkki K: Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 45: 528-537, 2000
13. Kaufmann SH, Gores GJ: Apoptosis in cancer: Cause and cure. Bioessays 22: 1007-1017, 2000
14. Aszalos A, Ross DD: Biochemical and clinical aspects of efflux pump related resistance to anti-cancer drugs. Anticancer Res 18: 2937-2944, 1998
15. Moscow JA et al.: Multidrug resistance. Cancer Chemother Biol Response Modif 17: 139-177, 1997
16. Reed JC: Mechanisms of apoptosis avoidance in cancer. Curr Opin Oncol 11: 68-75, 1999
17. Kastan MB, Canman CE, Leonard CJ: P53, cell cycle control and apoptosis: Implications for cancer. Cancer Metastasis Rev 14: 3-15, 1995
18. Langlois NE, Eremin O, Heys SD: Apoptosis and prognosis in cancer: Rationale and relevance. J R Coll Surg Edinb 45: 211-9, 2000
19. Ormerod MG: Flow Cytometry: A Practical Approach. 3rd edn., American Chemical Society, June 15, 2000, p 276
20. Darzynkiewicz Z, Tragos F: Measurement of apoptosis. In: Scheper T (ed) Advances in Biochemical Engineering/Biotechnology. 1998, pp 35-73
21. Matsumura K, Kawamoto K: Long-term passage results of glioma cells and their cell kinetics. Hum Cell 7: 158-166, 1994
22. Bedner E, Melamed MR, Darzynkiewicz Z: Enzyme kinetic reactions and fluorochrome uptake rates measured in individual cells by laser scanning cytometry. Cytometry 33: 1-9, 1998
23. Deptala A et al.: Activation of nuclear factor kappa B (NF-kappaB) assayed by laser scanning cytometry (LSC). Cytometry 33: 376-382, 1998
24. Deptala A, et al.: Differences in induction of p53, p21WAF1 and apoptosis in relation to cell cycle phase of MCF-7 cells treated with camptothecin. Int J Oncol 15: 861-871, 1999
25. Bedner E et al.: Translocation of Bax to mitochondria during apoptosis measured by laser scanning cytometry. Cytometry 41: 83-88, 2000
26. Abdel-Moneim I et al.: Proliferation and apoptosis in solid tumors. Analysis by laser scanning cytometry. Anal Quant Cytol Histol 22: 393-397, 2000
27. Clatch RJ, Foreman JR, Walloch JL: Simplified immunophenotypic analysis by laser scanning cytometry. Cytometry 34: 3-16, 1998
28. Darzynkiewicz Z, Bedner E: Analysis of apoptotic cells by flow and laser scanning cytometry. Methods Enzymol 322: 18-39, 2000
29. Furuya T et al.: Laser scanning cytometry allows detection of cell death with morphological features of apoptosis in cells stained with PI. Cytometry 29: 173-177, 1997
30. Li X, Melamed MR, Darzynkiewicz Z: Detection of apoptosis and DNA replication by differential labeling of DNA strand breaks with fluorochromes of different color. Exp Cell Res 222: 28-37, 1996
31. Liang BC, Ullyatt E: Chemosensitization of glioblastoma cells to bis-dichloroethyl-nitrosourea with tyrphostin AG17. Clin Cancer Res 4: 773-781, 1998
32. Miccoli L et al.: Potentiation of lonidamine and diazepam, two agents acting on mitochondria, in human glioblastoma treatment. J Natl Cancer Inst 90: 1400-1406, 1998
33. Ormerod MG et al.: Increased membrane permeability of apoptotic thymocytes: A flow cytometric study. Cytometry 14: 595-602, 1993
34. Wolter KG et al.: Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139: 1281-1292, 1997
35. Kamentsky LA, Kamentsky LD: Microscope-based multiparameter laser scanning cytometer yielding data comparable to flow cytometry data. Cytometry 12: 381-387, 1991
36. Kamentsky LA et al.: Slide-based laser scanning cytometry. Acta Cytol 41: 123-143, 1997
37. Darzynkiewicz Z et al.: Laser-scanning cytometry: A new instrumentation with many applications. Exp Cell Res 249: 1-12, 1999
38. Ormerod MG et al.: Discrimination of apoptotic thymocytes by forward light scatter. Cytometry 21: 300-304, 1995
39. Salzman GC, Singham SB, Johnston RG, Bohren CF: Light scattering and cytometry. In: Melamed MR, Lindmo T, Mendelsohn ML (eds) Flow Cytometry and Cell Sorting, Wiley-Liss, New York, 1990, pp 81-107
40. Oberhammer F et al.: Apoptotic death in epithelial cells: Cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. Embo J 12: 3679-3684, 1993
41. Kuribayashi N et al.: Chromatin structure and endonuclease sensitivity in human leukemic cell lines. Anticancer Res 16: 1225-1230, 1996
42. Iida M et al.: Endonuclease activity and hydrogen peroxide-induced cytotoxicity in human glioblastoma and glioma cell lines. Anticancer Res 19: 1235-1240, 1999
43. Gong J, Traganos F, Darzynkiewicz Z: A selective procedure for DNA extraction from apoptotic cells applicable for gel electrophoresis and flow cytometry. Anal Biochem 218: 317-319, 1994
44. Nicoletti I et al.: A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 139: 271-279, 1991
45. Honda C, Tabuchi K: Effects of cisplatin on cultured glioma cells. Gan To Kagaku Ryoho 13: 1921-1926, 1986
46. Kawamoto K: Flow cytometric analysis of cell cycle for the action mechanism of antineoplastic agents. Hum Cell 8: 85-88, 1995
47. Kin Y et al.: A novel role for the urokinase-type plasminogen activator receptor in apoptosis of malignant gliomas. Int J Oncol 17: 61-65, 2000
48. Bedner E et al.: Laser scanning cytometry distinguishes lymphocytes, monocytes, and granulocytes by differences in their chromatin structure. Cytometry 29: 191-196, 1997
49. Gold R et al.: Detection of DNA fragmentation in apoptosis: Application of in situ nick translation to cell culture systems and tissue sections. J Histochem Cytochem 41: 1023-1030, 1993
50. Li X et al.: Apoptotic cell death during treatment of leukemias. Leuk Lymphoma 13(Suppl. 2): 65-70, 1994
51. Seiter K et al.: Phase I clinical and laboratory evaluation of topotecan and cytarabine in patients with acute leukemia. J Clin Oncol 15: 44-51, 1997
52. Casper D et al.: Acetaminophen selectively reduces glioma cell growth and increases radiosensitivity in culture. J Neuro-Oncol 46: 215-229, 2000
53. Wang J et al.: Induction and characterization of human glioma clones with different radiosensitivities. Neoplasia 1 1: 138-144, 1999
54. Thomas LB et al.: DNA end labeling (TUNEL) in Huntington's disease and other neuropathological conditions. Exp Neurol 133: 265-272, 1995
55. Ehrmann J Jr, et al.: The expression of apoptosis-related proteins and the apoptotic rate in glial tumors of the brain. Neoplasma 47: 151-155, 2000
56. Ge S et al.: Carboxyamido-triazole induces apoptosis in bovine aortic endothelial and human glioma cells. Clin Cancer Res 6: 1248-1254, 2000
57. Gorczyca W et al.: Analysis of human tumors by laser scanning cytometry. Methods Cell Biol 64: 421-443, 2001
58. Darzynkiewicz Z, Li X: Measurements of cell death by flow cytometry, in Techniques in Apoptosis. A User's Guide, M.S. Cotter TG, Editor. Portland Press, London, 1996, 71-106
59. Darzynkiewicz Z et al.: Features of apoptotic cells measured by flow cytometry. Cytometry 13: 795-808, 1992
60. Darzynkiewicz Z, Li X, Gong J: Assays of cell viability: Discrimination of cells dying by apoptosis. Methods Cell Biol 41: 15-38, 1994
61. Hotz MA et al.: Flow cytometric detection of apoptosis: Comparison of the assays of in situ DNA degradation and chromatin changes. Cytometry 15: 237-244, 1994
62. Jurgensmeier JM et al.: Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 95(9): 4997-5002, 1998
63. Ikemoto H et al.: Calphostin C-mediated translocation and integration of Bax into mitochondria induces cytochrome c release before mitochondrial dysfunction. Cell Death Differ 7: 511-520, 2000
64. Darzynkiewicz Z: Acid-induced denaturation of DNA in situ as a probe of chromatin structure. Methods Cell Biol 41: 527-541, 1994
65. Frankfurt OS et al.: Apoptosis (programmed cell death) and the evaluation of chemosensitivity in chronic lymphocytic leukemia and lymphoma. Oncol Res 5: 37-42, 1993
66. Bowles AP et al.: Chemosensitivity testing of human gliomas using a fluorescent microcarrier technique. J Neuro-Oncol 8: 103-112, 1990
67. Fuse T et al.: Heat-induced apoptosis in human glioblastoma cell line A172. Neurosurgery 42: 843-849, 1998
68. Frey T: Nucleic acid dyes for detection of apoptosis in live cells. Cytometry 21: 265-274, 1995
69. Yin D, Tamaki N, Kokunai T: Wild-type p53-dependent etoposide-induced apoptosis mediated by caspase-3 activation in human glioma cells. J Neurosurg 93: 289-297, 2000
70. Fadok VA et al.: Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148: 2207-2216, 1992
71. Van Engeland M et al.: A novel assay to measure loss of plasma membrane asymmetry during apoptosis of adherent cells in culture. Cytometry 24: 131-139, 1996
72. Koopman G et al.: Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84: 1415-1420, 1994
73. Marchetti P et al.: Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 184: 1155-1160, 1996
74. Kawaguchi S et al.: Induction of apoptosis in glioma cells by recombinant human Fas ligand. Neurosurgery 46: 431-438; discussion 438-439, 2000
75. Van Engeland M et al.: Annexin V-affinity assay: A review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31: 1-9, 1998
76. Oliver FJ et al.: Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J Biol Chem 273: 33533-33539, 1998
77. Lautier D et al.: Molecular and biochemical features of poly (ADP-ribose) metabolism. Mol Cell Biochem 22: 171-193, 1993
78. Jeggo PA: DNA repair: PARP - Another guardian angel? Curr Biol 8(2): R49-51, 1998
79. Wang X et al.: Poly(ADP-ribosyl)ation is required for p53-dependent signal transduction induced by radiation. Oncogene 17: 2819-2825, 1998
80. Malapetsa A et al.: Identification of a 116 kDa protein able to bind 1,3-bis(2-chloroethyl)-1-nitrosourea-damaged DNA as poly(ADP-ribose) polymerase. Mutat Res 362: 41-50, 1996
81. Rice WG et al.: Induction of endonuclease-mediated apoptosis in tumor cells by C-nitroso-substituted ligands of poly(ADP-ribose) polymerase. Proc Natl Acad Sci USA 89: 7703-7707, 1992
82. Lazebnik YA et al.: Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371: 346-347, 1994
83. Ha HC, Snyder SH: Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA 96: 13978-13982, 1999
84. Bursztajn S et al.: Poly (ADP-ribose) polymerase induction is an early signal of apoptosis in human neuroblastoma. Brain Res Mol Brain Res 76: 363-376, 2000
85. Sallmann FR et al.: Characterization of antibodies specific for the caspase cleavage site on poly(ADP-ribose) polymerase: Specific detection of apoptotic fragments and mapping of the necrotic fragments of poly(ADP-ribose) polymerase. Biochem Cell Biol 75: 451-456, 1997
86. Affar EB et al.: Immunological determination and size characterization of poly(ADP-ribose) synthesized in vitro and in vivo. Biochim Biophys Acta 1428: 137-146, 1999
87. Li X, Darzynkiewicz Z: Cleavage of Poly(ADP-ribose) polymerase measured in situ in individual cells: Relationship to DNA fragmentation and cell cycle position during apoptosis. Exp Cell Res 255: 125-132, 2000
88. Duriez PJ et al.: Characterization of anti-peptide antibodies directed towards the automodification domain and apoptotic fragment of poly (ADP-ribose) polymerase. Biochim Biophys Acta 1334: 65-72, 1997
89. Duriez PJ, Shah GM: Cleavage of poly(ADP-ribose) polymerase: A sensitive parameter to study cell death. Biochem Cell Biol 75: 337-349, 1997
90. Li X, Du L, Darzynkiewicz Z: During apoptosis of HL-60 and U-937 cells caspases are activated independently of dissipation of mitochondrial electrochemical potential. Exp Cell Res 257: 290-297, 2000
91. Hermisson M et al.: Sensitization to CD95 ligand-induced apoptosis in human glioma cells by hyperthermia involves enhanced cytochrome c release. Oncogene 19: 2338-2345, 2000
92. Hirsch T et al.: The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15: 1573-1581, 1997
93. Shinoura N et al.: Adenovirus-mediated transfer of bax with caspase-8 controlled by myelin basic protein promoter exerts an enhanced cytotoxic effect in gliomas. Cancer Gene Ther 7: 739-748, 2000
94. Slee EA et al.: Ordering the cytochrome c-initiated caspase cascade: Hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144: 281-292, 1999
95. Castedo M et al.: Sequential acquisition of mitochondrial and plasma membrane alterations during early lymphocyte apoptosis. J Immunol 157: 512-521, 1996
96. Lizard G et al.: Kinetics of plasma membrane and mitochondrial alterations in cells undergoing apoptosis. Cytometry 21: 275-283, 1995
97. Darzynkiewicz Z et al.: Interaction of rhodamine 123 with living cells studied by flow cytometry. Cancer Res 42: 799-806, 1982
98. Bedner E et al.: Analysis of apoptosis by laser scanning cytometry. Cytometry 35: 181-195, 1999
99. Vogelbaum MA et al.: Overexpression of bax in human glioma cell lines. J Neurosurg 91: 483-489, 1999
100. Alnemri ES et al.: Human ICE/CED-3 protease nomenclature. Cell 87: 171, 1996
101. Kaufmann SH et al.: Specific proteolytic cleavage of poly(ADP-ribose) polymerase: An early marker of chemotherapy-induced apoptosis. Cancer Res 53: 3976-3985, 1993
102. Liu J et al.: Fluorescent molecular probes V: A sensitive caspase-3 substrate for fluorometric assays. Bioorg Med Chem Lett 9: 3231-3236, 1999
103. Hug H et al.: Rhodamine 110-linked amino acids and peptides as substrates to measure caspase activity upon apoptosis induction in intact cells. Biochemistry 38: 13906-13911, 1999
104. Gorman AM et al.: Application of a fluorometric assay to detect caspase activity in thymus tissue undergoing apoptosis in vivo. J Immunol Methods 226: 43-48, 1999
105. Earnshaw WC, Martins LM, Kaufmann SH: Mammalian caspases: Structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68: 383-424, 1999
106. Bedner E et al.: Activation of caspases measured in situ by binding of fluorochrome-labeled inhibitors of caspases (FLICA): Correlation with DNA fragmentation. Exp Cell Res 259: 308-313, 2000
107. Zhivotovsky B et al.: Caspases: Their intracellular localization and translocation during apoptosis. Cell Death Differ 6: 644-651, 1999
108. Budihardjo I et al.: Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol. 15: 269-290, 1999
109. Beg AA, Baltimore D: An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274: 782-784, 1996
110. Otsuka G et al.: Inhibition of nuclear factor-kappaB activation confers sensitivity to tumor necrosis factor-alpha by impairment of cell cycle progression in human glioma cells. Cancer Res 59: 4446-4452, 1999
111. Boland MP, Foster SJ, O'Neill LA: Daunorubicin activates NFkappaB and induces kappaB-dependent gene expression in HL-60 promyelocytic and Jurkat T lymphoma cells. J Biol Chem 272: 12952-12960, 1997
112. Nagata S: Apoptosis by death factor. Cell 88: 355-365, 1997
113. Baeuerle PA, Henkel T: Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12: 141-179, 1994
114. Baldwin AS Jr: The NF-kappa B I kappa B proteins: New discoveries and insights. Annu Rev Immunol 14: 649-683, 1996
115. Siebenlist U, Franzoso G, Brown K: Structure, regulation and function of NF-kappa B. Annu Rev Cell Biol 10: 405-455, 1994
116. Miyakoshi J, Yagi K: Inhibition of I kappaB-alpha phosphorylation at serine and tyrosine acts independently on sensitization to DNA damaging agents in human glioma cells. Br J Cancer 82: 28-33, 2000
117. Lahiri DK, Ge Y: Electrophoretic mobility shift assay for the detection of specific DNA-protein complex in nuclear extracts from the cultured cells and frozen autopsy human brain tissue. Brain Res Brain Res Protoc 5: 257-265, 2000
118. Lopes UG et al.: p53-dependent induction of apoptosis by proteasome inhibitors. J Biol Chem 272: 12893-12896, 1997
119. Olson DC, Levine AJ: The properties of p53 proteins selected for the loss of suppression of transformation. Cell Growth Differ 5: 61-71, 1994
120. Kubbutat MH, Vousden KH: Proteolytic cleavage of human p53 by calpain: A potential regulator of protein stability. Mol Cell Biol 17: 460-468, 1997
121. Anker L et al.: p53 protein accumulation and gene mutations in human glioma cell lines. Int J Cancer 55: 982-987, 1993
122. Zhan Q et al.: Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis. Oncogene 9: 3743-3751, 1994
123. Musco ML et al.: Comparison of flow cytometry and laser scanning cytometry for the intracellular evaluation of adenoviral infectivity and p53 protein expression in gene therapy. Cytometry 33: 290-296, 1998
124. Korshunov A et al.: Prognostic value of tumour associated antigen immunoreactivity and apoptosis in cerebral glioblastomas: An analysis of 168 cases. J Clin Pathol 52: 574-580, 1999
125. Gorczyca W, Darzynkiewicz Z, Melamed MR: Laser scanning cytometry in pathology of solid tumors. A review. Acta Cytol 41: 98-108, 1997
126. Clatch RJ, Walloch JL: Multiparameter immunophenotypic analysis of fine needle aspiration biopsies and other hematologic specimens by laser scanning cytometry. Acta Cytol 41: 109-122, 1997
127. Li X et al.: Apoptotic cell death during treatment of leukemias. Leuk Lymphoma 13(Suppl. 1): 65-70, 1994
128. Seiter K et al.: Evaluation of in vivo induction of apoptosis in patients with acute leukemia treated on a phase I study of paclitaxel. Leukemia 9: 1961-1966, 1995
129. Maciorowski Z et al.: Comparative analysis of apoptosis measured by Hoechst and flow cytometry in non-Hodgkin's lymphomas. Cytometry 32: 44-50, 1998
130. Ehrmann J Jr. et al.: The expression of apoptosis-related proteins and the apoptotic rate in glial tumors of the brain. Neoplasma 47: 151-155, 2000
131. Casper D et al.: Acetaminophen selectively reduces glioma cell growth and increases radiosensitivity in culture. J Neuro-Oncol 46: 215-229, 2000
132. Heesters MA et al.: Analysis of proliferation and apoptosis in brain gliomas: Prognostic and clinical value. J Neuro-Oncol 44: 255-266, 1999
133. Krajewski S 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 150: 805-814, 1997
134. McPake CR et al.: Bax is an important determinant of chemosensitivity in pediatric tumor cell lines independent of Bcl-2 expression and p53 status. Oncol Res 10: 235-244, 1998
135. Weller M et al.: Anti-Fas/APO-1 antibody-mediated apoptosis of cultured human glioma cells. Induction and modulation of sensitivity by cytokines. J Clin Invest 94: 954-964, 1994
136. Roth W et al.: Immunochemotherapy of malignant glioma: Synergistic activity of CD95 ligand and chemotherapeutics. Cancer Immunol Immunother 44: 55-63, 1997
137. Gratas C et al.: Fas ligand expression in glioblastoma cell lines and primary astrocytic brain tumors. Brain Pathol 7: 863-869, 1997
138. Glaser T et al.: Death receptor-independent cytochrome c release and caspase activation mediate thymidine kinase plus ganciclovir-mediated cytotoxicity in LN-18 and LN-229 human malignant glioma cells. Gene Ther 8: 469-476, 2001
139. Shinoura N et al.: Adenovirus-mediated transfer of fas ligand gene augments radiation-induced apoptosis in U-373MG glioma cells [In Process Citation]. Jpn J Cancer Res 91: 1044-1050, 2000
140. Shinoura N et al.: Adenovirus-mediated overexpression of fas induces apoptosis of gliomas. Cancer Gene Ther 7: 224-232, 2000.