Anti-Fas/APO-1 antibody-mediated apoptosis of cultured human glioma cells: Induction and modulation of sensitivity by cytokines

Journal of Clinical Investigation

Volumn 94, Issue 3, 1994, Pages 954-964

  Weller, Michael ^a   Frei, Karl ^a   Groscurth, Peter ^a   Krammer, Peter H ^b   Yonekawa, Yasuhiro ^a   Fontana, Adriano ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Apoptosis; Fas APO 1; Glioma; Immunotherapy; TNF

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; COLONY STIMULATING FACTOR 1; CYCLOHEXIMIDE; CYTOKINE; DACTINOMYCIN; GROWTH FACTOR RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 8; LYMPHOTOXIN; NERVE GROWTH FACTOR; RECOMBINANT GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 1BETA; RECOMBINANT INTERLEUKIN 2; RECOMBINANT INTERLEUKIN 4; RECOMBINANT INTERLEUKIN 6; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA2;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; APOPTOSIS; ARTICLE; CANCER IMMUNOTHERAPY; CENTRAL NERVOUS SYSTEM TUMOR; CONTROLLED STUDY; FLOW CYTOMETRY; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RNA SYNTHESIS;

ANTIBODIES; ANTIGENS, CD95; ANTIGENS, SURFACE; APOPTOSIS; CELL LINE; CYTOKINES; DNA, NEOPLASM; FLOW CYTOMETRY; GLIOMA; HUMAN; IMMUNOHISTOCHEMISTRY; INTERFERON-GAMMA, RECOMBINANT; INTERLEUKINS; LIPOPOLYSACCHARIDES; MACROPHAGE COLONY-STIMULATING FACTOR; MICROSCOPY, ELECTRON; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; SUPPORT, NON-U.S. GOV'T; TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR;

EID: 0027990763     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI117462     Document Type: Article

References (61)

1. Deen, F. D., A. Chiarado, E. A. Grimm, J. R. Fike, M. A. Israel, L. E. Kun, V. A. Levin, L. J. Marton, R. J. Packer, A. E. Pegg, M. L. Rosenblum, H. D. Suit, M. D. Walker, C. J. Wikstrand, C. B. Wilson, A. J. Wong, and W. K. A. Yung. 1993. Brain tumor working group report on the 9th International Conference on Brain Tumor Research and Therapy. J. Neuro-Oncol. 16:243-272.
2. Korsmeyer, S. J. 1992. Bcl-2: an antidote to programmed cell death. Cancer Surv. 15:105-118.
3. Kerr, J. F. R., A. H. Wyllie, and A. R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26:239-257.
4. Cohen, J. J. 1993. Apoptosis. Immunol. Today. 14:126-130.
5. Schwartz, L. M., and B. A. Osborne. 1993. Programmed cell death, apoptosis and killer genes. Immunol. Today. 14:582-590.
6. Schwartzman, R. A., and J. A. Cidlowski. 1993. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr. Rev. 14:133-151.
7. Barry, M. A., C. A. Behnke, and A. Eastman. 1990. Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins and hyperthermia. Biochem. Pharmacol. 40:2353-2362.
8. Sen, S., and M. D'Incalci. 1992. Apoptosis. Biochemical events and relevance to cancer chemotherapy. FEBS (Fed. Eur. Biochem. Soc.) Lett. 307:122-127.
9. Reed, J. C. 1994. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1-6.
10. Yonehara, S., A. Ishii, and M. Yonehara. 1989. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J. Exp. Med. 169:1747-1756.
11. Trauth, B. C., C. Klas, A. M. J. Peters, S. Matzku, P. Möller, W. Falk, K. M. Debatin, and P. H. Krammer. 1989. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science (Wash. DC). 245:301-305.
12. Itoh, N., S. Yonehara, A. Ishii, M. Yonehara, S. I. Mizushima, M. Sameshima, A. Hase, Y. Seto, and S. Nagata. 1991. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell. 66:233-243.
13. Oehm, A., I. Behrmann, W. Falk, M. Pawlita, G. Maier, C. Klas, M. Li-Wever, S. Richards, J. Dhein, B. C. Trauth, H. Ponstingl, and P. H. Krammer. 1992. Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/nerve growth factor receptor superfamily. Sequence identity with the Fas antigen. J. Biol. Chem. 267:10709-10715.
14. Itoh, N., and S. Nagata. 1993. A novel protein domain required for apoptosis. Mutational analysis of human fas antigen. J. Biol Chem. 268:10932-10937.
15. Tartaglia, L. A., T. M. Ayres, G. H. W. Wong, and D. V. Goeddel. 1993. A novel domain within the 55 kd TNF receptor signals cell death. Cell. 74:845-853.
16. Watanabe-Fukunaga, R., C. I. Brannan, N. G. Copeland, N. A. Jenkins, and S. Nagata. 1992. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature (Lond.). 356:314-317.
17. Debatin, K. M., D. Süss, and P. H. Krammer. 1994. Differential expression of APO-1 on human thymocytes: implications for negative selection. Eur. J. Immunol. 24:753-758.
18. Rouvier, E., M. L. Luciani, and P. Golstein. 1993. Fas involvement in Ca2+-independent T cell-mediated cytotoxicity. J. Exp. Med. 177:195-200.
19. Leithäuser, F., J. Dhein, G. Mechtersheimer, K. Koretz, S. Brüderlein, C. Henne, A. Schmidt, K. M. Debatin, P. H. Krammer, and P. Möller. 1993. Constitutive and induced expression of APO-1, a new member of the nerve growth factor/ tumor necrosis factor receptor superfamily, in normal and neoplastic cells. Lab. Invest. 69:415-429.
20. Dhein, J., P. T. Daniel, B. C. Trauth, A. Oehm, P. Möller, and P. H. Krammer. 1992. Induction of apoptosis by monoclonal antibody anti-APO-1 class switch variants is dependent on cross-linking of APO-1 cell surface antigens. J. Immunol. 149:3166-3173.
21. Suda, T., T. Takahashi, P. Golstein, and S. Nagata. 1993. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell. 75:1169-1178.
22. Suda, T., and S. Nagata. 1994. Purification and characterization of the Fas-ligand that induces apoptosis. J. Exp. Med. 179:873-879.
23. Fontana, A., W. Fierz, and H. Wekerle. 1984. Astrocytes present myelin basic protein to encephalitogenic T-cell lines. Nature (Lond.). 307:273-276.
24. Fontana, A., H. Hengartner, N. de Tribolet, and E. Weber. 1984. Glioblastoma cells release interleukin 1 and factors inhibiting interleukin 2-mediated effects. J. Immunol. 132:1837-1844.
25. Bodmer, S., K. Strommer, K. Frei, C. Siepl, N. de Tribolet, I. Heid, and A. Fontana. 1989. Immunosuppression and transforming growth factor-β in glioblastoma. Preferential production of transforming growth factor-β2. J. Immunol. 143:3222-3229.
26. Constam, D. B., J. Philipp, U. V. Malipiero, P. Ten Dijke, M. Schachner, and A. Fontana. 1992. Differential expression of transforming growth factor-β1, β2, and β3 by glioblastoma cells, astrocytes, and microglia. J. Immunol. 148:1404-1410.
27. Frei, K., D. Piani, U. V. Malipiero, E. Van Meir, N. de Tribolet, and A. Fontana. 1992. Granulocyte-macrophage colony-stimulating factor (GM-CSF) production by glioblastoma cells. Despite the presence of inducing signals GM-CSF is not expressed in vivo. J. Immunol. 148:3140-3146.
28. Frei, K., C. Siepl, P. Groscurth, S. Bodmer, C. Schwerdel, and A. Fontana. 1987. Antigen presentation and tumor cytotoxicity by interferon-γ-treated microglial cells. Eur. J. Immunol. 17:1271-1278.
29. 2 induces apoptosis of murine T cell clones without down-regulating bcl-2 mRNA expression. Eur. J. Immunol. 24:1293-1300.
30. Gavrieli, Y., Y. Sherman, and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear fragmentation. J. Cell Biol. 119:493-501.
31. Shi, Y., M. G. Szalay, L. Paskar, M. Boyer, B. Singh, and D. R. Green. 1990. Activation-induced cell death in T cell hybridomas is due to apoptosis. Morphologic aspects and DNA fragmentation. J. Immunol. 144:3326-3333.
32. Arends, M. J., R. G. Morris, and A. H. Wyllie. 1990. Apoptosis. The role of the endonuclease. Am. J. Pathol. 136:593-608.
33. Zuber, P., R. S. Accolla, S. Carrel, A. C. Diserens, and N. de Tribolet. 1988. Effects of recombinant human tumor necrosis factor-α on the surface phenotype and the growth of human malignant glioma cell lines. Int. J. Cancer. 42:780-786.
34. Larrick, J. W., and S. C. Wright. 1990. Cytotoxic mechanism of tumor necrosis factor-α. FASEB (Fed. Am. Soc. Exp. Biol.) J. 4:3215-3223.
35. Vassalli, P. 1992. The pathophysiology of tumor necrosis factors. Annu. Rev. Immunol. 10:411-452.
36. Morimoto, H., S. Yonehara, and B. Bonavida. 1993. Overcoming tumor necrosis factor and drug resistance of human tumor cell lines by combination treatment with anti-fas antibody and drugs or toxins. Cancer Res. 53:2591-2596.
37. Watanabe-Fukunaga, R., C. I. Brennan, N. Itoh, S. Yonehara, N. G. Copeland, N. A. Jenkins, and S. Nagata. 1992. The cDNA structure, expression, and chromosomal assignment of the mouse Fas antigen. J. Immunol. 148:1274-1279.
38. Maxwell, M., T. Galanopoulos, J. Neville-Golden, and H. N. Antoniades. 1992. Effect of the expression of transforming growth factor-β2 in primary human glioblastomas on immunosuppression and loss of immune surveillance. J. Neurosurg. 76:799-784.
39. Black, K. L., K. Chen, D. P. Becker, and J. E. Merril. 1992. Inflammatory leukocytes associated with increased immunosuppression by glioblastoma. J. Neurosurg. 77:120-126.
40. 1 in human astrocytomas. Hum. Pathol. 23:1284-1288.
41. Schneider, J., F. M. Hofman, M. L. J. Apuzzo, and D. R. Hinton. 1992. Cytokines and immunoregulatory molecules in malignant glial neoplasms. J. Neurosurg. 77:265-273.
42. Tada, M., Y. Sawamura, S. Sakuma, K. Suzuki, H. Ohta, T. Aida, and H. Abe. 1993. Cellular and cytokine responses of the human central nervous system to intracranial administration of tumor necrosis factor α for the treatment of malignant gliomas. Cancer Immunol. Immunother. 36:251-259.
43. Tada, T., K. Yabu, and S. Kobayashi. 1993. Detection of active form of transforming growth factor-β in cerebrospinal fluid of patients with glioma. JPN. J. Cancer Res. 84:544-548.
44. Ruffini, P. A., L. Rivoltini, A. Silvani, A. Boiardi, and G. Parmiani. 1993. Factors, including transforming growth factor β, released in the glioblastoma residual cavity, impair activity of adherent lymphokine-activated killer cells. Cancer Immunol. Immunother. 36:409-416.
45. Van Meir, E., M. Ceska, F. Effenberger, A. Walz, E. Grouzman, I. Desbaillets, K. Frei, A. Fontana, and N. de Tribolet. 1992. Interleukin-8 is produced in neoplastic and infectious diseases of the human central nervous system. Cancer Res. 52:4297-4305.
46. Owen-Schaub, L. B., S. Meterissian, and R. J. Ford. 1993. Fas/APO-1 expression and function on malignant cells of hematologic and nonhematologic origin. J. Immunotherapy. 14:234-241.
47. Möller, P., C. Henne, F. Leithäuser, A. Eichelmann, A. Schmidt, S. Brüderlein, J. Dhein, and P. H. Krammer. 1993. Coregulation of the APO-1 antigen with intercellular adhesion molecule-1 (CD54) in tonsillar B cells and coordinate expression in follicular center B cells and in follicle center and mediastinal B-cell lymphomas. Blood. 81:2067-2075.
48. Miyawaki, T., T. Uehara, R. Nibu, T. Tsuji, A. Yachie, S. Yonehara, and N. Taniguchi. 1992. Differential expression of apoptosis-related fas antigen on lymphocyte subpopulations in human peripheral blood. J. Immunol. 149:3753-3758.
49. Klas, C., K. M. Debatin, R. R. Jonker, and P. H. Krammer. 1993. Activation interferes with the APO-1 pathway in mature human T cells. Int. Immunol. 5:625-630.
50. Falk, M. H., B. C. Trauth, K. M. Debatin, C. Klas, C. D. Gregory, A. B. Rickinson, A. Calender, G. M. Lenoir, J. W. Ellwart, P. H. Krammer, and G. W. Bomkamm. 1992. Expression of the APO-1 antigen in Burkitt lymphoma cell lines correlates with a shift towards a lymphoblastoid phenotype. Blood. 79:3300-3306.
51. Mapara, M. Y., R. Bargou, C. Zugck, H. Döhner, F. Ustaoglu, R. R. Jonker, P. H. Krammer, and B. Dörken. 1993. APO-1 mediated apoptosis or proliferation in human chronic B lymphocytic leukemia: correlation with bcl-2 oncogene expression. Eur. J. Immunol. 23:702-708.
52. Alderson, M. R., R. J. Armitage, E. Maraskovsky, T. W. Tough, E. Roux, K. Schooley, F. Ramsdell, and D. H. Lynch. 1993. Fas transduces activation signals in normal human T lymphocytes. J. Exp. Med. 178:2231-2235.
53. Wong, G. H. W., J. H. Elwell, L. W. Oberley, and D. V. Goeddel. 1989. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell. 58:923-931.
54. Itoh, N., Y. Tsujimoto, and S. Nagata, 1993. Effect of bcl-2 on Fas antigen-mediated cell death. J. Immunol. 151:621-627.
55. Hockenbery, D. M., Z. N. Oltvai, X. M. Yin, C. L. Milliman, and S. J. Korsmeyer. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75:241-251.
56. Vanhaesebroeck, B., J. C. Reed, D. De Valck, J. Grooten, T. Miyashita, S. Tanaka, R. Beyaert, F. Van Roy, and W. Fiers. 1993. Effect of bcl-2 protooncogene expression on cellular sensitivity to tumor necrosis factor-mediated cytotoxicity. Oncogene. 8:1075-1081.
57. Vaux, D. L., H. L. Aguila, and I. L. Weissman. 1992. Bcl-2 prevents death of factor-deprived cells but fails to prevent apoptosis in targets of cell mediated killing. Int. Immunol. 4:821-824.
58. Hockenbery, D. M., M. Zutter, W. Hickey, M. Nahm, and S. J. Korsmeyer. 1991. BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc. Natl. Acad. Sci. USA. 88:6961-6965.
59. Hall, W. A., and Ø. Fodstad. 1992. Immunotoxins and central nervous system neoplasia. J. Neurosurg. 76:1-12.
60. Yoshida, J., T. Wakabayashi, M. Mizuno, K. Sugita, T. Yoshida, S. Hori, T. Mori, T. Sato, A. Karashima, K. Kurisu, K. Kiya, and T. Uozumi. 1992. Clinical effect of intra-arterial tumor necrosis factor-α for malignant glioma. J. Neurosurg. 77:78-83.
61. Ogasawara, J., R. Watanabe-Fukunaga, M. Adachi, A. Matsuzawa, T. Kasugai, Y. Kitamura, N. Itoh, T. Suda, and S. Nagata. 1993. Lethal effect of the anti-Fas antibody in mice. Nature (Lond.). 364:806-809.