Retinoic acid regulates Fas-induced apoptosis in Jurkat T cells: Reversal of mitogen-mediated repression of Fas DISC assembly

Journal of Leukocyte Biology

Volumn 85, Issue 3, 2009, Pages 469-480

  Engedal, Nikolai ^a,b   Auberger, Patrick ^c   Blomhoff, Heidi Kiil ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c INSERM   (France)

Author keywords

Caspase 8; Concanavalin A; Phorbol ester

Indexed keywords

ALITRETINOIN; CASPASE 6; CONCANAVALIN A; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; DNA; DOUBLE STRANDED DNA; FAS ANTIGEN; FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHORBOL 13 ACETATE 12 MYRISTATE; PROCASPASE 3; PROCASPASE 8; RETINOIC ACID;

APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE DEPOLARIZATION; CELL PROTECTION; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS REACTION; DNA FRAGMENTATION; DOUBLE STRANDED DNA BREAK; DRUG EFFECT; DRUG MECHANISM; ELECTROPORATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LEUKEMIA CELL LINE; LIPID RAFT; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CLEAVAGE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANTIGENS, CD95; APOPTOSIS; CASPASE 8; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; JURKAT CELLS; LEUKEMIA; MITOGENS; NF-KAPPA B; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRETINOIN;

EID: 61449142531     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1107790     Document Type: Article

References (80)

1. Nagata, S. (1999) Fas ligand-induced apoptosis. Annu. Rev. Genet. 33, 29-55.
2. Peter, M. E., Krammer, P. H. (2003) The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ. 10, 26-35.
3. Boatright, K. M., Salvesen, G. S. (2003) Mechanisms of caspase activation. Curr. Opin. Cell Biol. 15, 725-731.
4. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. M., Krammer, P. H., Peter, M. E. (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17, 1675-1687.
5. Barnhart, B. C., Alappat, E. C., Peter, M. E. (2003) The CD95 type I/type II model. Semin. Immunol. 15, 185-193.
6. Stennicke, H. R., Jurgensmeier, J. M., Shin, H., Deveraux, Q., Wolf, B. B., Yang, X., Zhou, Q., Ellerby, H. M., Ellerby, L. M., Bredesen, D., Green, D. R., Reed, J. C., Froelich, C. J., Salvesen, G. S. (1998) Pro-caspase-3 is a major physiologic target of caspase-8. J. Biol. Chem. 273, 27084-27090.
7. Eguchi, Y., Srinivasan, A., Tomaselli, K. J., Shimizu, S., Tsujimoto, Y. (1999) ATP-dependent steps in apoptotic signal transduction. Cancer Res. 59, 2174-2181.
8. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489.
9. Scaffidi, C., Schmitz, I., Zha, J., Korsmeyer, S. J., Krammer, P. H., Peter, M. E. (1999) Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. J. Biol. Chem. 274, 22532-22538.
10. Westendorp, M. O., Frank, R., Ochsenbauer, C., Stricker, K., Dhein, J., Walczak, H., Debatin, K. M., Krammer, P. H. (1995) Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375, 497-500.
11. Peter, M. E., Kischkel, F. C., Scheuerpflug, C. G., Medema, J. P., Debatin, K. M., Krammer, P. H. (1997) Resistance of cultured peripheral T cells towards activation-induced cell death involves a lack of recruitment of FLICE (MACH/caspase 8) to the CD95 death-inducing signaling complex. Eur. J. Immunol. 27, 1207-1212.
12. Klas, C., Debatin, K. M., Jonker, R. R., Krammer, P. H. (1993) Activation interferes with the APO-1 pathway in mature human T cells. Int. Immunol. 5, 625-630.
13. Dhein, J., Walczak, H., Baumler, C., Debatin, K. M., Krammer, P. H. (1995) Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 373, 438-441.
14. Zheng, L., Fisher, G., Miller, R. E., Peschon, J., Lynch, D. H., Lenardo, M. J. (1995) Induction of apoptosis in mature T cells by tumor necrosis factor. Nature 377, 348-351.
15. Pender, M. P. (1999) Activation-induced apoptosis of autoreactive and alloreactive T lymphocytes in the target organ as a major mechanism of tolerance. Immunol. Cell Biol. 77, 216-223.
16. Straus, S. E., Jaffe, E. S., Puck, J. M., Dale, J. K., Elkon, K. B., Rosen-Wolff, A., Peters, A. M., Sneller, M. C., Hallahan, C. W., Wang, J., Fischer, R. E., Jackson, C. M., Lin, A. Y., Baumler, C., Siegert, E., Marx, A., Vaishnaw, A. K., Grodzicky, T., Fleisher, T. A., Lenardo, M. J. (2001) The development of lymphomas in families with autoimmune lymphoproliferative syndrome with germline Fas mutations and defective lymphocyte apoptosis. Blood 98, 194-200.
17. Zhang, Y., Finegold, M. J., Porteu, F., Kanteti, P., Wu, M. X. (2003) Development of T-cell lymphomas in Emu-IEX-1 mice. Oncogene 22, 6845-6851.
18. Nagata, S. (1998) Human autoimmune lymphoproliferative syndrome, a defect in the apoptosis-inducing Fas receptor: a lesson from the mouse model. J. Hum. Genet. 43, 2-8.
19. Stephensen, C. B. (2001) Vitamin A, infection, and immune function. Annu. Rev. Nutr. 21, 167-192.
20. Valone, F. H., Payan, D. G. (1985) Potentiation ofmitogen-induced human T-lymphocyte activation by retinoic acid. Cancer Res. 45, 4128-4131.
21. Yang, Y., Bailey, J., Vacchio, M. S., Yarchoan, R., Ashwell, J. D. (1995) Retinoic acid inhibition of ex vivo human immunodeficiency virus-associated apoptosis of peripheral blood cells. Proc. Natl. Acad. Sci. USA 92, 3051-3055.
22. Szondy, Z., Lecoeur, H., Fesus, L., Gougeon, M. L. (1998) All-trans retinoic acid inhibition of anti-CD3-induced T cell apoptosis in human immunodeficiency virus infection mostly concerns CD4 T lymphocytes and is mediated via regulation of CD95 ligand expression. J. Infect. Dis. 178, 1288-1298.
23. Ertesvag, A., Engedal, N., Naderi, S., Blomhoff, H. K. (2002) Retinoic acid stimulates the cell cycle machinery in normal T cells: involvement of retinoic acid receptor-mediated IL-2 secretion. J. Immunol. 169, 5555-5563.
24. Engedal, N., Ertesvag, A., Blomhoff, H. K. (2004) Survival of activated human T lymphocytes is promoted by retinoic acid via induction of IL-2. Int. Immunol. 16, 443-453.
25. Engedal, N., Gjevik, T., Blomhoff, R., Blomhoff, H. K. (2006) All-trans retinoic acid stimulates IL-2-mediated proliferation of human T lymphocytes: early induction of cyclin D3. J. Immunol. 177, 2851-2861.
26. Hayes, C. E., Nashold, F. E., Enrique Gomez, F., Hoag, K. A. (1999). Retinoids and immunity. In Retinoids: The Biochemical and Molecular-Basis of Vitamin A and Retinoid Action (H. Nau, W. S. Blaner, eds.), Springer-Verlag, Berlin 589-610.
27. Wei, L. N. (2003) Retinoid receptors and their coregulators. Annu. Rev. Pharmacol. Toxicol. 43, 47-72.
28. Holmstrom, T. H., Chow, S. C., Elo, I., Coffey, E. T., Orrenius, S., Sistonen, L., Eriksson, J. E. (1998) Suppression of Fas/APO-1-mediated apoptosis by mitogen-activated kinase signaling. J. Immunol. 160, 2626-2636.
29. Engedal, N., Blomhoff, H. K. (2003) Combined action of ERK and NF κB mediates the protective effect of phorbol ester on Fas-induced apoptosis in Jurkat cells. J. Biol. Chem. 278, 10934-10941.
30. Herrant, M., Luciano, F., Loubat, A., Auberger, P. (2002) The protective effect of phorbol esters on Fas-mediated apoptosis in T cells. Transcrip-tional and posttranscriptional regulation. Oncogene 21, 4957-4968.
31. Yeh, J. H., Hsu, S. C., Han, S. H., Lai, M. Z. (1998) Mitogen-activated protein kinase kinase antagonized Fas-associated death domain protein-mediated apoptosis by induced FLICE-inhibitory protein expression. J. Exp. Med. 188, 1795-1802.
32. Yonehara, S., Ishii, A., Yonehara, M. (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.
33. Jodo, S., Strehlow, D., Ju, S. T. (2000) Bioactivities of Fas ligandexpressing retroviral particles. J. Immunol. 164, 5062-5069.
34. Weiss, A., Wiskocil, R. L., Stobo, J. D. (1984) The role of T3 surface molecules in the activation of human T cells: a two-stimulus requirement for IL 2 production reflects events occurring at a pre-translational level. J. Immunol. 133, 123-128.
35. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
36. Yang, Y., Vacchio, M. S., Ashwell, J. D. (1993) 9-cis-retinoic acid inhibits activation-driven T-cell apoptosis: implications for retinoid X receptor involvement in thymocyte development. Proc. Natl. Acad. Sci. USA 90, 6170-6174.
37. Yang, Y., Minucci, S., Ozato, K., Heyman, R. A., Ashwell, J. D. (1995) Efficient inhibition of activation-induced Fas ligand up-regulation and T cell apoptosis by retinoids requires occupancy of both retinoid X receptors and retinoic acid receptors. J. Biol. Chem. 270, 18672-18677.
38. Wyllie, A. H., Kerr, J. F., Currie, A. R. (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251-306.
39. Gorczyca, W., Bigman, K., Mittelman, A., Ahmed, T., Gong, J., Melamed, M. R., Darzynkiewicz, Z. (1993) Induction of DNA strand breaks associated with apoptosis during treatment of leukemias. Leukemia 7, 659-670.
40. Marchetti, P., Castedo, M., Susin, S. A., Zamzami, N., Hirsch, T., Macho, A., Haeffner, A., Hirsch, F., Geuskens, M., Kroemer, G. (1996) Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med. 184, 1155-1160.
41. Salvioli, S., Ardizzoni, A., Franceschi, C., Cossarizza, A. (1997) JC-1, but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess δ ψ changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett. 411, 77-82.
42. Kroemer, G., Zamzami, N., Susin, S. A. (1997) Mitochondrial control of apoptosis. Immunol. Today 18, 44-51.
43. Nakagawa, S., Fujii, T., Yokoyama, G., Kazanietz, M. G., Yamana, H., Shirouzu, K. (2003) Cell growth inhibition by all-trans retinoic acid in SKBR-3 breast cancer cells: involvement of protein kinase Cα and extra-cellular signal-regulated kinase mitogen-activated protein kinase. Mol. Carcinog. 38, 106-116.
44. Dalvin, S., Komatsuzaki, K., Anselmo, M. A., Kling, D. E., Schnitzer, J. J., Kinane, T. B. (2004) Retinoic acid decreases fetal lung mesenchymal cell proliferation in vivo and in vitro. Dev. Growth Differ. 46, 275-282.
45. Na, S. Y., Kang, B. Y., Chung, S. W., Han, S. J., Ma, X., Trinchieri, G., Im, S. Y., Lee, J. W., Kim, T. S. (1999) Retinoids inhibit interleukin-12 production in macrophages through physical associations of retinoid X receptor and NFκJ. Biol. Chem. 274, 7674-7680.
46. Lewis, T. S., Shapiro, P. S., Ahn, N. G. (1998) Signal transduction through MAP kinase cascades. Adv. Cancer Res. 74, 49-139.
47. Slee, E. A., Harte, M. T., Kluck, R. M., Wolf, B. B., Casiano, C. A., Newmeyer, D. D., Wang, H. G., Reed, J. C., Nicholson, D. W., Alnemri, E. S., Green, D. R., Martin, S. J. (1999) 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.
48. Wolf, B. B., Schuler, M., Echeverri, F., Green, D. R. (1999) Caspase-3 is the primary activator of apoptotic DNA fragmentation via DNA fragmentation factor-45/inhibitor of caspase-activated DNase inactivation. J. Biol. Chem. 274, 30651-30656.
49. Gomez-Angelats, M., Cidlowski, J. A. (2001) Protein kinase C regulates FADD recruitment and death-inducing signaling complex formation in Fas/CD95-induced apoptosis. J. Biol. Chem. 276, 44944-44952.
50. Meng, X. W., Heldebrant, M. P., Kaufmann, S. H. (2002) Phorbol 12-myristate 13-acetate inhibits death receptor-mediated apoptosis in Jurkat cells by disrupting recruitment of Fas-associated polypeptide with death domain. J. Biol. Chem. 277, 3776-3783.
51. Cowling, V., Downward, J. (2002) Caspase-6 is the direct activator of caspase-8 in the cytochrome c-induced apoptosis pathway: absolute requirement for removal of caspase-6 prodomain. Cell Death Differ. 9, 1046-1056.
52. Kischkel, F. C., Hellbardt, S., Behrmann, I., Germer, M., Pawlita, M., Krammer, P. H., Peter, M. E. (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J. 14, 5579-5588.
53. Algeciras-Schimnich, A., Shen, L., Barnhart, B. C., Murmann, A. E., Burkhardt, J. K., Peter, M. E. (2002) Molecular ordering of the initial signaling events of CD95. Mol. Cell. Biol. 22, 207-220.
54. Holler, N., Tardivel, A., Kovacsovics-Bankowski, M., Hertig, S., Gaide, O., Martinon, F., Tinel, A., Deperthes, D., Calderara, S., Schulthess, T., Engel, J., Schneider, P., Tschopp, J. (2003) Two adjacent trimeric Fas ligands are required for Fas signaling and formation of a death-inducing signaling complex. Mol. Cell. Biol. 23, 1428-1440.
55. Feig, C., Tchikov, V., Schutze, S., Peter, M. E. (2007) Palmitoylation of CD95 facilitates formation of SDS-stable receptor aggregates that initiate apoptosis signaling. EMBO J. 26, 221-231.
56. Varadhachary, A. S., Edidin, M., Hanlon, A. M., Peter, M. E., Krammer, P. H., Salgame, P. (2001) Phosphatidylinositol 3'-kinase blocks CD95 aggregation and caspase-8 cleavage at the death-inducing signaling complex by modulating lateral diffusion of CD95. J. Immunol. 166, 6564-6569.
57. Ducoroy P., Micheau O., Perruche S., Dubrez-Daloz L., de Fornel, D., Dutartre P., Saas P., Solary E. (2003) LF 15-0195 immunosuppressive agent enhances activation-induced T-cell death by facilitating caspase-8 and caspase-10 activation at the DISC level. Blood 101, 194-201.
58. Chakrabandhu, K., Herincs, Z., Huault, S., Dost, B., Peng, L., Concho-naud, F., Marguet, D., He, H. T., Hueber, A. O. (2007) Palmitoylation is required for efficient Fas cell death signaling. EMBO J. 26, 209-220.
59. Cahuzac, N., Baum, W., Kirkin, V., Conchonaud, F., Wawrezinieck, L., Marguet, D., Janssen, O., Zornig, M., Hueber, A. O. (2006) Fas ligand is localized to membrane rafts, where it displays increased cell death-inducing activity. Blood 107, 2384-2391.
60. Simons, K., Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
61. Christian, A. E., Haynes, M. P., Phillips, M. C., Rothblat, G. H. (1997) Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 38, 2264-2272.
62. Orlandi, P. A., Fishman, P. H. (1998) Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141, 905-915.
63. De Kruijff, B., Demel, R. A. (1974) Polyene antibiotic-sterol interactions in membranes of Acholeplasma laidlawii cells and lecithin liposomes. 3. Molecular structure of the polyene antibiotic-cholesterol complexes. Bio-chim. Biophys. Acta 339, 57-70.
64. Valavanis, C., Hu, Y., Yang, Y., Osborne, B. A., Chouaib, S., Greene, L., Ashwell, J. D., Schwartz, L. M. (2001) Model cell lines for the study of apoptosis in vitro. Methods Cell Biol. 66, 417-436.
65. Holmstrom, T. H., Schmitz, I., Soderstrom, T. S., Poukkula, M., Johnson, V. L., Chow, S. C., Krammer, P. H., Eriksson, J. E. (2000) MAPK/ERK signaling in activated T cells inhibits CD95/Fas-mediated apoptosis downstream of DISC assembly. EMBO J. 19, 5418-5428.
66. Kamitani, T., Nguyen, H. P., Yeh, E. T. (1997) Activation-induced aggregation and processing of the human Fas antigen. Detection with cytoplasmic domain-specific antibodies. J. Biol. Chem. 272, 22307-22314.
67. Papoff, G., Hausler, P., Eramo, A., Pagano, M. G., Di, L. G., Signore, A., Ruberti, G. (1999) Identification and characterization of a ligand-inde-pendent oligomerization domain in the extracellular region of the CD95 death receptor. J. Biol. Chem. 274, 38241-38250.
68. Lautrette, C., Loum-Ribot, E., Petit, D., Vermot-Desroches, C., Wijdenes, J., Jauberteau, M. O. (2006) Increase of Fas-induced apoptosis by inhibition of extracellular phosphorylation of Fas receptor in Jurkat cell line. Apoptosis 11, 1195-1204.
69. Muppidi, J. R., Tschopp, J., Siegel, R. M. (2004) Life and death decisions: secondary complexes and lipid rafts in TNF receptor family signal trans-duction. Immunity 21, 461-465.
70. Chaigne-Delalande, B., Moreau, J. F., Legembre, P. (2008) Rewinding the DISC. Arch. Immunol. Ther. Exp. (Warsz.) 56, 9-14.
71. Muppidi, J. R., Siegel, R. M. (2004) Ligand-independent redistribution of Fas (CD95) into lipid rafts mediates clonotypic T cell death. Nat. Immunol. 5, 182-189.
72. Bissonnette, R. P., Brunner, T., Lazarchik, S. B., Yoo, N. J., Boehm, M. F., Green, D. R., Heyman, R. A. (1995) 9-cis retinoic acid inhibition of activation-induced apoptosis is mediated via regulation of Fas ligand and requires retinoic acid receptor and retinoid X receptor activation. Mol. Cell. Biol. 15, 5576-5585.
73. Cui, H., Sherr, D. H., el-Khatib, M., Matsui, K., Panka, D. J., Marshak-Rothstein, A., Ju, S. T. (1996) Regulation of T-cell death genes: selective inhibition of FasL-but not Fas-mediated function. Cell. Immunol. 167, 276-284.
74. Toth, B., Ludanyi, K., Kiss, I., Reichert, U., Michel, S., Fesus, L., Szondy, Z. (2004) Retinoids induce Fas(CD95) ligand cell surface expression via RARγ and nur77 in T cells. Eur. J. Immunol. 34, 827-836.
75. Zapata, J. M., Reed, J. C. (2002) TRAF1: lord without a RING. Sci. STKE 2002, PE27.
76. Sax, J. K., El-Deiry, W. S. (2003) Identification and characterization of the cytoplasmic protein TRAF4 as a p53-regulated proapoptotic gene. J. Biol. Chem. 278, 36435-36444.
77. Proft, T., Fraser, J. D. (2003) Bacterial superantigens. Clin. Exp. Immunol. 133, 299-306.
78. Altucci, L., Gronemeyer, H. (2001) The promise of retinoids to fight against cancer. Nat. Rev. Cancer 1, 181-193.
79. Clarke, N., Nebbioso, A., Altucci, L., Gronemeyer, H. (2005) TRAIL: at the center of drugable anti-tumor pathways. Cell Cycle 4, 914-918.
80. Harper, N., Hughes, M. A., Farrow, S. N., Cohen, G. M., MacFarlane, M. (2003) Protein kinase C modulates tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by targeting the apical events of death receptor signaling. J. Biol. Chem. 278, 44338-44347.