The CD95 (APO-1/Fas) and the TRAIL (APO-2L) apoptosis systems

Experimental Cell Research

Volumn 256, Issue 1, 2000, Pages 58-66

  Walczak, Henning ^a   Krammer, Peter H ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ANTIGEN;

APOPTOSIS; INHIBITION KINETICS; LIVER METABOLISM; PRIORITY JOURNAL; REGULATORY MECHANISM; SHORT SURVEY; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

EID: 0034630161     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.2000.4840     Document Type: Article

References (105)

1. Trauth B. C., Klas C., Peters A. M., Matzku S., Möller P., Falk W., Debatin K. M., Krammer P. H. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science. 245:1989;301-305.
2. 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. 169:1989;1747-1756.
3. Itoh N., Yonehara S., Ishii A., Yonehara M., Mizushima S., Sameshima M., Hase A., Seto Y., Nagata S. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell. 66:1991;233-243.
4. Oehm A., Behrmann I., Falk W., Pawlita M., Maier G., Klas C., Li-Weber M., Richards S., Dhein J., Trauth B. C. 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. 267:1992;10709-10715.
5. Schlossman S. F., Boumsell L., Gilks W., Harlan J.M., Kishimoto T., Morimoto C., Ritz J., Shaw S., Silverstein R., Springer T., Tedder T. F., Todd R. F. White Cell Differentiation Antigens. Proceedings of the Fifth International Workshop and Conference. Leucocyte Typing V. 1995;Oxford Univ. Press.
6. Cheng J., Zhou T., Liu C., Shapiro J. P., Brauer M. J., Kiefer M. C., Barr P. J., Mountz J. D. Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. Science. 263:1994;1759-1762.
7. Lichter P., Walczak H., Weitz S., Behrmann I., Krammer P. H. The human APO-1 (APT) antigen maps to 10q23, a region that is syntenic with mouse chromosome 19. Genomics. 14:1992;179-180.
8. Watanabe-Fukunaga R., Brannan C. I., Itoh N., Yonehara S., Copeland N. G., Jenkins N. A., Nagata S. The cDNA structure, expression, and chromosomal assignment of the mouse Fas antigen. J. Immunol. 148:1992;1274-1279.
9. Klas C., Debatin K. M., Jonker R. R., Krammer P. H. Activation interferes with the APO-1 pathway in mature human T cells. Int. Immunol. 5:1993;625-630.
10. Möller P., Koretz K., Leithäuser F., Brüderlein S., Henne C., Quentmeier A., Krammer P. H. Expression of APO-1 (CD95), a member of the NGF/TNF receptor superfamily, in normal and neoplastic colon epithelium. Int. J. Cancer. 57:1994;371-377.
11. Leithäuser F., Dhein J., Mechtersheimer G., Koretz K., Brüderlein S., Henne C., Schmidt A., Debatin K. M., Krammer P. H., Möller P. 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. 69:1993;415-429.
12. 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. 75:1993;1169-1178.
13. Takahashi T., Tanaka M., Brannan C. I., Jenkins N. A., Copeland N. G., Suda T., Nagata S. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell. 76:1994;969-976.
14. Takahashi T., Tanaka M., Inazawa J., Abe T., Suda T., Nagata S. Human Fas ligand: Gene structure, chromosomal location and species specificity. Int. Immunol. 6:1994;1567-1574.
15. Anel A., Simon A. K., Auphan N., Buferne M., Boyer C., Golstein P., Schmitt-Verhulst A. M. Two signaling pathways can lead to Fas ligand expression in CD8+ cytotoxic T lymphocyte clones. Eur. J. Immunol. 25:1995;3381-3387.
16. Tanaka M., Suda T., Takahashi T., Nagata S. Expression of the functional soluble form of human fas ligand in activated lymphocytes. Embo J. 14:1995;1129-1135.
17. Tanaka M., Suda T., Haze K., Nakamura N., Sato K., Kimura F., Motoyoshi K., Mizuki M., Tagawa S., Ohga S., Hatake K., Drummond A. H., Nagata S. Fas ligand in human serum. Nat. Med. 2:1996;317-322.
18. Tanaka M., Suda T., Yatomi T., Nakamura N., Nagata S. Lethal effect of recombinant human Fas ligand in mice pretreated with Propionibacterium acnes. J. Immunol. 158:1997;2303-2309.
19. Tanaka M., Itai T., Adachi M., Nagata S. Downregulation of Fas ligand by shedding. Nat. Med. 4:1998;31-36.
20. Krammer P. H., Dhein J., Walczak H., Behrmann I., Mariani S., Matiba B., Fath M., Daniel P. T., Knipping E., Westendorp M. O. The role of APO-1-mediated apoptosis in the immune system. Immunol. Rev. 142:1994;175-191.
21. Nagata S., Golstein P. The Fas death factor. Science. 267:1995;1449-1456.
22. Peter M. E., Scaffidi C., Medema J. P., Kischkel F., Krammer P. H. The death receptors. Results Prob. Cell Differ. 23:1999;25-63.
23. Suda T., Hashimoto H., Tanaka M., Ochi T., Nagata S. Membrane Fas ligand kills human peripheral blood T lymphocytes, and soluble Fas ligand blocks the killing. J. Exp. Med. 186:1997;2045-2050.
24. Dhein J., Walczak H., Bäumler C., Debatin K. M., Krammer P. H. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95) [see comments]. Nature. 373:1995;438-441.
25. Rothstein T. L., Wang J. K., Panka D. J., Foote L. C., Wang Z., Stanger B., Cui H., Ju S. T., Marshak-Rothstein A. Protection against Fas-dependent Th1-mediated apoptosis by antigen receptor engagement in B cells. Nature. 374:1995;163-165.
26. French L. E., Hahne M., Viard I., Radlgruber G., Zanone R., Becker K., Muller C., Tschopp J. Fas and Fas ligand in embryos and adult mice: ligand expression in several immune-privileged tissues and coexpression in adult tissues characterized by apoptotic cell turnover. J. Cell. Biol. 133:1996;335-343.
27. Ni R., Tomita Y., Matsuda K., Ichihara A., Ishimura K., Ogasawara J., Nagata S. Fas-mediated apoptosis in primary cultured mouse hepatocytes. Exp. Cell Res. 215:1994;332-337.
28. Galle P. R., Hofmann W. J., Walczak H., Schaller H., Otto G., Stremmel W., Krammer P. H., Runkel L. Involvement of the CD95 (APO-1/Fas) receptor and ligand in liver damage. J. Exp. Med. 182:1995;1223-1230.
29. Adachi M., Suematsu S., Kondo T., Ogasawara J., Tanaka T., Yoshida N., Nagata S. Targeted mutation in the Fas gene causes hyperplasia in peripheral lymphoid organs and liver. Nat. Genet. 11:1995;294-300.
30. Dhein J., Daniel P. T., Trauth B. C., Oehm A., Möller P., Krammer P. H. 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. 149:1992;3166-3173.
31. Banner D. W., D'Arcy A., Janes W., Gentz R., Schoenfeld H. J., Broger C., Loetscher H., Lesslauer W. Crystal structure of the soluble human 55 kd TNF receptor-human TNF beta complex: Implications for TNF receptor activation. Cell. 73:1993;431-445.
32. Tartaglia L. A., Ayres T. M., Wong G. H., Goeddel D. V. A novel domain within the 55 kd TNF receptor signals cell death. Cell. 74:1993;845-853.
33. Itoh N., Tsujimoto Y., Nagata S. Effect of bcl-2 on Fas antigen-mediated cell death. J. Immunol. 151:1993;621-627.
34. Chinnaiyan A. M., O'Rourke K., Tewari M., Dixit V. M. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell. 81:1995;505-512.
35. Boldin M. P., Varfolomeev E. E., Pancer Z., Mett I. L., Camonis J. H., Wallach D. A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J. Biol. Chem. 270:1995;7795-7798.
36. Stanger B. Z., Leder P., Lee T. H., Kim E., Seed B. RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell. 81:1995;513-523.
37. Cuppen E., Nagata S., Wieringa B., Hendriks W. No evidence for involvement of mouse protein-tyrosine phosphatase-BAS- like Fas-associated phosphatase-1 in Fas-mediated apoptosis. J. Biol. Chem. 272:1997;30215-30220.
38. Kolesnick R. N., Haimovitz-Friedman A., Fuks Z. The sphingomyelin signal transduction pathway mediates apoptosis for tumor necrosis factor, Fas, and ionizing radiation. Biochem Cell Biol. 72:1994;471-474.
39. Cifone M. G., De Maria R., Roncaioli P., Rippo M. R., Azuma M., Lanier L. L., Santoni A., Testi R. Apoptotic signaling through CD95 (Fas/Apo-1) activates an acidic sphingomyelinase. J. Exp. Med. 180:1994;1547-1552.
40. Tepper C. G., Jayadev S., Liu B., Bielawska A., Wolff R., Yonehara S., Hannun Y. A., Seldin M. F. Role for ceramide as an endogenous mediator of Fas-induced cytotoxicity. Proc. Natl. Acad. Sci. USA. 92:1995;8443-8447.
41. Eischen C. M., Dick C. J., Leibson P. J. Tyrosine kinase activation provides an early and requisite signal for Fas-induced apoptosis. J. Immunol. 153:1994;1947-1954.
42. Zhou T., Song L., Yang P., Wang Z., Lui D., Jope R. S. Bisindolylmaleimide VIII facilitates Fas-mediated apoptosis and inhibits T cell-mediated autoimmune diseases. Nat. Med. 5:1999;42-48.
43. Copeland K. F., Haaksma A. G., Goudsmit J., Krammer P. H., Heeney J. L. Inhibition of apoptosis in T cells expressing human T cell leukemia virus type I Tax. AIDS Res. Hum. Retroviruses. 10:1994;1259-1268.
44. Huang B., Eberstadt M., Olejniczak E. T., Meadows R. P., Fesik S. W. NMR structure and mutagenesis of the Fas (APO-1/CD95) death domain. Nature. 384:1996;638-641.
45. Kischkel F. C., Hellbardt S., Behrmann I., Germer M., Pawlita M., Krammer P. H., Peter M. E. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. Embo J. 14:1995;5579-5588.
46. Chinnaiyan A. M., Tepper C. G., Seldin M. F., O'Rourke K., Kischkel F. C., Hellbardt S., Krammer P. H., Peter M. E., Dixit V. M. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271:1996;4961-4965.
47. Muzio M., Chinnaiyan A. M., Kischkel F. C., O'Rourke K., Shevchenko A., Ni J., Scaffidi C., Bretz J. D., Zhang M., Gentz R., Mann M., Krammer P. H., Peter M. E., Dixit V. M. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death - inducing signaling complex. Cell. 85:1996;817-827.
48. Boldin M. P., Goncharov T. M., Goltsev Y. V., Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell. 85:1996;803-815.
49. Fernandes-Alnemri T., Armstrong R. C., Krebs J., Srinivasula S. M., Wang L., Bullrich F., Fritz L. C., Trapani J. A., Tomaselli K. J., Litwack G., Alnemri E. S. In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc. Natl. Acad. Sci. USA. 93:1996;7464-7469.
50. Alnemri E. S., Livingston D. J., Nicholson D. W., Salvesen G., Thornberry N. A., Wong W. W., Yuan J. Human ICE/CED-3 protease nomenclature. Cell. 87:1996;171.
51. Medema J. P., Scaffidi C., Kischkel F. C., Shevchenko A., Mann M., Krammer P. H., Peter M. E. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). Embo J. 16:1997;2794-2804.
52. Scaffidi C., Medema J. P., Krammer P. H., Peter M. E. FLICE is predominantly expressed as two functionally active isoforms, caspase-8/a and caspase-8/b. J. Biol. Chem. 272:1997;26953-26958.
53. Srinivasula S. M., Ahmad M., Fernandes-Alnemri T., Litwack G., Alnemri E. S. Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple Ced-3/ICE-like cysteine proteases. Proc. Natl. Acad. Sci. USA. 93:1996;14486-14491.
54. Muzio M., Salvesen G. S., Dixit V. M. FLICE induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J. Biol. Chem. 272:1997;2952-2956.
55. Medema J. P., Toes R. E., Scaffidi C., Zheng T. S., Flavell R. A., Melief C. J., Peter M. E., Offringa R., Krammer P. H. Cleavage of FLICE (caspase-8) by granzyme B during cytotoxic T lymphocyte-induced apoptosis. Eur. J. Immunol. 27:1997;3492-3498.
56. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K. J., Debatin K. M., Krammer P. H., Peter M. E. Two CD95 (APO-1/Fas) signaling pathways. Embo J. 17:1998;1675-1687.
57. Schmitz I., Walczak H., Krammer P. H., Peter M. E. Differences between CD95 type I and II cells detected with the CD95 ligand. Cell Death Differ. 6:1999;821-822.
58. Li H., Zhu H., Xu C. J., Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
59. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:1998;481-490.
60. L. Proc. Natl. Acad. Sci. USA. 96:1999;14871-14876.
61. Peter M. E., Medema J. P., Krammer P. H. Does the Caenorhabditis elegans protein CED-4 contain a region of homology to the mammalian death effector domain. Cell Death Diff. 4:1997;523-525.
62. Thome M., Schneider P., Hofmann K., Fickenscher H., Meinl E., Neipel F., Mattmann C., Burns K., Bodmer J. L., Schroter M., Scaffidi C., Krammer P. H., Peter M. E., Tschopp J. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature. 386:1997;517-521.
63. Hu S., Vincenz C., Ni J., Gentz R., Dixit V. M. I-FLICE, a novel inhibitor of tumor necrosis factor receptor-1- and CD-95-induced apoptosis. J. Biol. Chem. 272:1997;17255-17257.
64. Bertin J., Armstrong R. C., Ottilie S., Martin D. A., Wang Y., Banks S., Wang G. H., Senkevich T. G., Alnemri E. S., Moss B., Lenardo M. J., Tomaselli K. J., Cohen J. I. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. Proc. Natl. Acad. Sci. USA. 94:1997;1172-1176.
65. Irmler M., Thome M., Hahne M., Schneider P., Hofmann K., Steiner V., Bodmer J. L., Schroter M., Burns K., Mattmann C., Rimoldi D., French L. E., Tschopp J. Inhibition of death receptor signals by cellular FLIP. Nature. 388:1997;190-195.
66. Srinivasula S. M., Ahmad M., Ottilie S., Bullrich F., Banks S., Wang Y., Fernandes-Alnemri T., Croce C. M., Litwack G., Tomaselli K. J., Armstrong R. C., Alnemri E. S. FLAME-1, a novel FADD-like anti-apoptotic molecule that regulates Fas/TNFR1-induced apoptosis. J. Biol. Chem. 272:1997;18542-18545.
67. Shu H. B., Halpin D. R., Goeddel D. V. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity. 6:1997;751-763.
68. Goltsev Y. V., Kovalenko A. V., Arnold E., Varfolomeev E. E., Brodianskii V. M., Wallach D. CASH, a novel caspase homologue with death effector domains. J. Biol. Chem. 272:1997;19641-19644.
69. Rasper D. M., Vaillancourt J. P., Hadano S., Houtzager V. M., Seiden I., Keen S. L., Tawa P., Xanthoudakis S., Nasir J., Martindale D., Koop B. F., Peterson E. P., Thornberry N. A., Huang J., MacPherson D. P., Black S. C., Hornung F., Lenardo M. J., Hayden M. R., Roy S., Nicholson D. W. Cell death attenuation by "Usurpin," a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death Differ. 5:1998;271-288.
70. Inohara N., Koseki T., Hu Y., Chen S., Nunez G. CLARP, a death effector domain-containing protein interacts with caspase-8 and regulates apoptosis. Proc. Natl. Acad. Sci. USA. 94:1997;10717-10722.
71. L and initiates cell death. Proc. Natl. Acad. Sci. USA. 94:1997;11333-11338.
72. Kischkel F. C., Kioschis P., Weitz S., Poustka A., Lichter P., Krammer P. H. Assignment of CASP8 to human chromosome band 2q33 → q34 and Casp8 to the murine syntenic region on chromosome 1B-proximal C by in situ hybridization. Cytogenet Cell Genet. 82:1998;95-96.
73. Wiley S. R., Schooley K., Smolak P. J., Din W. S., Huang C. P., Nicholl J. K., Sutherland G. R., Smith T. D., Rauch C., Smith C. A. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity. 3:1995;673-682.
74. Degli-Esposti M. To die or not to die - The quest of the TRAIL receptors. J. Leukoc. Biol. 65:1999;535-542.
75. Emery J. G., McDonnell P., Burke M. B., Deen K. C., Lyn S., Silverman C., Dul E., Appelbaum E. R., Eichman C., DiPrinzio R., Dodds R. A., James I. E., Rosenberg M., Lee J. C., Young P. R. Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J. Biol. Chem. 273:1998;14363-14367.
76. Pan G., Ni J., Wei Y. F., Yu G., Gentz R., Dixit V. M. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science. 277:1997;815-818.
77. Sheridan J. P., Marsters S. A., Pitti R. M., Gurney A., Skubatch M., Baldwin D., Ramakrishnan L., Gray C. L., Baker K., Wood W. I., Goddard A. D., Godowski P., Ashkenazi A. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science. 277:1997;818-821.
78. Thomas W. D., Hersey P. TNF-related apoptosis-inducing ligand (TRAIL) induces apoptosis in Fas ligand-resistant melanoma cells and mediates CD4 T cell killing of target cells. J. Immunol. 161:1998;2195-2200.
79. Griffith T. S., Chin W. A., Jackson G. C., Lynch D. H., Kubin M. Z. Intracellular regulation of TRAIL-induced apoptosis in human melanoma cells. J. Immunol. 161:1998;2833-2840.
80. Zhang X. D., Franco A., Myers K., Gray C., Nguyen T., Hersey P. Relation of TNF-related apoptosis-inducing ligand (TRAIL) receptor and FLICE-inhibitory protein expression to TRAIL-induced apoptosis of melanoma. Cancer Res. 59:1999;2747-2753.
81. Leverkus M., Neumann M., Mengling T., Rauch C. T., Bröcker E.-B., Krammer P. H., Walczak H. Regulation of TRAIL sensitivity in primary and transformed human keratinocytes. Cancer Res. 60:2000;553-559.
82. Leverkus, M, Walczak, H, Fries, W.-H, Terbeck, G, McLellan, A, Broecker, E.-B, and, Kaempgen, E. Maturation of dendritic cells leads to upregulation of cellular-Flice-inhibitory Protein (c-FLIP) and concomitant downregulation of death-ligand-mediated apoptosis. Submitted.
83. Weigand, M. A, Sprick, M. R, Grosse-Wilde, A, Krammer, P. H, and, Walczak, H. Differential Regulation of the CD95- and TRAIL-System on Human Peripheral T Lymphocytes. Submitted.
84. Mariani S. M., Matiba B., Armandola E. A., Krammer P. H. Interleukin 1 beta-converting enzyme related proteases/caspases are involved in TRAIL-induced apoptosis of myeloma and leukemia cells. J. Cell Biol. 137:1997;221-229.
85. L. Submitted.
86. Lynch, D. H. Immunol. Today, in press.
87. Sprick, M. R, Weigand, M. A, Juo, P, Blenis, J, Rauch, C. T, Krammer, P. H, and, Walczak, H. Caspase-8 and FADD/Mort1 are essential components of the TRAIL-R2 Death-Inducing Signalling Complex (DISC). Submitted.
88. Griffith T. S., Wiley S. R., Kubin M. Z., Sedger L. M., Maliszewski C. R., Fanger N. A. Monocyte-mediated tumoricidal activity via the tumor necrosis factor-related cytokine, TRAIL. J. Exp. Med. 189:1999;1343-1354.
89. Sedger L. M., Shows D. M., Blanton R. A., Peschon J. J., Goodwin R. G., Cosman D., Wiley S. R. IFN-gamma mediates a novel antiviral activity through dynamic modulation of TRAIL and TRAIL receptor expression. J. Immunol. 163:1999;920-926.
90. Musgrave B. L., Phu T., Butler J. J., Makrigiannis A. P., Hoskin D. W. Murine TRAIL (TNF-related apoptosis inducing ligand) expression induced by T cell activation is blocked by rapamycin, cyclosporin A, and inhibitors of phosphatidylinositol 3-kinase, protein kinase C, and protein tyrosine kinases: evidence for TRAIL induction via the T cell receptor signaling pathway. Exp. Cell Res. 252:1999;96-103.
91. Kayagaki N., Yamaguchi N., Nakayama M., Takeda K., Akiba H., Tsutsui H., Okamura H., Nakanishi K., Okumura K., Yagita H. Expression and function of TNF-related apoptosis-inducing ligand on murine activated NK cells. J. Immunol. 163:1999;1906-1913.
92. Kayagaki N., Yamaguchi N., Nakayama M., Eto H., Okumura K., Yagita H. Type I interferons (IFNs) regulate tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) expression on human T cells: A novel mechanism for the antitumor effects of type I IFNs. J. Exp. Med. 189:1999;1451-1460.
93. Mariani S. M., Krammer P. H. Surface expression of TRAIL/Apo-2 ligand in activated mouse T and B cells. Eur. J. Immunol. 28:1998;1492-1498.
94. Martinez-Lorenzo M. J., Anel A., Gamen S., Monle N. I., Lasierra P., Larrad L., Pineiro A., Alava M. A., Naval J. Activated human T cells release bioactive Fas ligand and APO2 ligand in microvesicles. J. Immunol. 163:1999;1274-1281.
95. Kayagaki N., Yamaguchi N., Nakayama M., Kawasaki A., Akiba H., Okumura K., Yagita H. Involvement of TNF-related apoptosis-inducing ligand in human CD4+ T cell-mediated cytotoxicity. J. Immunol. 162:1999;2639-2647.
96. Fanger N. A., Maliszewski C. R., Schooley K., Griffith T. S. Human dendritic cells mediate cellular apoptosis via tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J. Exp. Med. 190:1999;1155-1164.
97. Vidalain P. O., Azocar O., Lamouille B., Astier A., Rabourdin-Combe C., Servet-Delprat C. Measles virus induces functional TRAIL production by human dendritic cells. J. Virol. 74:2000;556-559.
98. Zamai L., Ahmad M., Bennett I. M., Azzoni L., Alnemri E. S., Perussia B. Natural killer (NK) cell-mediated cytotoxicity: Differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. J. Exp. Med. 188:1998;2375-2380.
99. Johnsen A. C., Haux J., Steinkjer B., Nonstad U., Egeberg K., Sundan A., Ashkenazi A., Espevik T. Regulation of APO-2 ligand/trail expression in NK cells-involvement in NK cell-mediated cytotoxicity. Cytokine. 11:1999;664-672.
100. Kashii Y., Giorda R., Herberman R. B., Whiteside T. L., Vujanovic N. L. Constitutive expression and role of the TNF family ligands in apoptotic killing of tumor cells by human NK cells. J. Immunol. 163:1999;5358-5366.
101. Wu G. S., Burns T. F., Zhan Y., Alnemri E. S., El-Deiry W. S. Molecular cloning and functional analysis of the mouse homologue of the KILLER/DR5 tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor. Cancer Res. 59:1999;2770-2775.
102. Walczak H., Miller R. E., Ariail K., Gliniak B., Griffith T. S., Kubin M., Chin W., Jones J., Woodward A., Le T., Smith C., Smolak P., Goodwin R. G., Rauch C. T., Schuh J. C., Lynch D. H. Tumoricidal activity of tumor necrosis factor-related apoptosis- inducing ligand in vivo. Nat. Med. 5:1999;157-163.
103. Pitti R. M., Marsters S. A., Ruppert S., Donahue C. J., Moore A., Ashkenazi A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271:1996;12687-12690.
104. Ashkenazi A., Pai R. C., Fong S., Leung S., Lawrence D. A., Marsters S. A., Blackie C., Chang L., McMurtrey A. E., Hebert A., DeForge L., Koumenis I. L., Lewis D., Harris L., Bussiere J., Koeppen H., Shahrokh Z., Schwall R. H. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104:1999;155-162.
105. Bonavida B., Ng C. P., Jazirehi A., Schiller G., Mizutani Y. Selectivity of TRAIL-mediated apoptosis of cancer cells and synergy with drugs: The trail to non-toxic cancer therapeutics. Int. J. Oncol. 15:1999;793-802.