Signaling active CD95 receptor molecules trigger co-translocation of inactive CD95 molecules into lipid rafts

Journal of Biological Chemistry

Volumn 287, Issue 28, 2012, Pages 24026-24042

  Lang, Isabell ^a   Fick, Andrea ^a   Schäfer, Viktoria ^a   Giner, Tina ^a   Siegmund, Daniela ^a   Wajant, Harald ^a  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATED SIGNALING; BINDING STUDIES; HEXAMERS; INACTIVE RECEPTORS; LIPID RAFT; MEMBRANE FRACTION; N-TERMINALS;

GENETIC ENGINEERING; OLIGOMERIZATION; OLIGOMERS;

MOLECULES;

CASPASE 8; CD40 RECEPTOR; CD95 RECEPTOR; FAS LIGAND; INTERLEUKIN 8; LUCIFERASE; LYMPHOCYTE ANTIGEN RECEPTOR; RECOMBINANT ANTIGEN; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; BINDING ASSAY; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENETIC ENGINEERING; INTRACELLULAR TRANSPORT; LIPID RAFT; MOLECULAR RECOGNITION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; RECEPTOR UPREGULATION; REPORTER GENE; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION;

ANTIGENS, CD40; ANTIGENS, CD95; APOPTOSIS; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; CYCLOHEXIMIDE; FAS LIGAND PROTEIN; HEK293 CELLS; HUMANS; JURKAT CELLS; KINETICS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SOLUBILITY;

GAUSSIA PRINCEPS (T. SCOTT, 1894);

EID: 84863624064     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.328211     Document Type: Article

References (64)

1. Locksley, R. M., Killeen, N., and Lenardo, M. J. (2001) The TNF and TNF receptor superfamilies. Integrating mammalian biology. Cell 104, 487-501 (Pubitemid 32201945)
2. Sancho-Martinez, I., and Martin-Villalba, A. (2009) Tyrosine phosphorylation and CD95. A FAScinating switch. Cell Cycle 8, 838-842
3. Wajant, H., Pfizenmaier, K., and Scheurich, P. (2003) Non-apoptotic Fas signaling. Cytokine Growth Factor Rev. 14, 53-66 (Pubitemid 36098431)
4. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S., Bodmer, J. L., Schneider, P., Seed, B., and Tschopp, J. (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1, 489-495
5. Kreuz, S., Siegmund, D., Rumpf, J. J., Samel, D., Leverkus, M., Janssen, O., Häcker, G., Dittrich-Breiholz, O., Kracht, M., Scheurich, P., and Wajant, H. (2004) NFκB activation by Fas is mediated through FADD, caspase-8, and RIP and is inhibited by FLIP. J. Cell Biol. 166, 369-380 (Pubitemid 39031240)
6. Bodmer, J. L., Schneider, P., and Tschopp, J. (2002) The molecular architecture of the TNF superfamily. Trends Biochem. Sci. 27, 19-26 (Pubitemid 34131621)
7. 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., and 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 (Pubitemid 36177050)
8. Schneider, P., Holler, N., Bodmer, J. L., Hahne, M., Frei, K., Fontana, A., and Tschopp, J. (1998) Conversion of membrane-bound Fas(CD95) ligand to its soluble form is associated with down-regulation of its proapoptotic activity and loss of liver toxicity. J. Exp. Med. 187, 1205-1213 (Pubitemid 28189110)
9. Suda, T., Hashimoto, H., Tanaka, M., Ochi, T., and Nagata, S. (1997) Membrane Fas ligand kills human peripheral blood T lymphocytes, and soluble Fas ligand blocks the killing. J. Exp. Med. 186, 2045-2050 (Pubitemid 28013689)
10. Tanaka, M., Itai, T., Adachi, M., and Nagata, S. (1998) Down-regulation of Fas ligand by shedding. Nat. Med. 4, 31-36
11. Bremer, E., ten Cate, B., Samplonius, D. F., de Leij, L. F., and Helfrich, W. (2006) CD7-restricted activation of Fas-mediated apoptosis. A novel therapeutic approach for acute T-cell leukemia. Blood 107, 2863-2870
12. Bremer, E., ten Cate, B., Samplonius, D. F., Mueller, N., Wajant, H., Stel, A. J., Chamuleau, M., van de Loosdrecht, A. A., Stieglmaier, J., Fey, G. H., and Helfrich, W. (2008) Superior activity of fusion protein scFvRit:sFasL over cotreatment with rituximab and Fas agonists. Cancer Res. 68, 597-604 (Pubitemid 351380089)
13. Samel, D., Muller, D., Gerspach, J., Assohou-Luty, C., Sass, G., Tiegs, G., Pfizenmaier, K., and Wajant, H. (2003) Generation of a FasL-based proapoptotic fusion protein devoid of systemic toxicity due to cell-surface antigen-restricted activation. J. Biol. Chem. 278, 32077-32082 (Pubitemid 37048396)
14. Herrero, R., Kajikawa, O., Matute-Bello, G., Wang, Y., Hagimoto, N., Mongovin, S., Wong, V., Park, D. R., Brot, N., Heinecke, J. W., Rosen, H., Goodman, R. B., Fu, X., and Martin, T. R. (2011) The biological activity of FasL in human and mouse lungs is determined by the structure of its stalk region. J. Clin. Invest. 121, 1174-1190
15. Aoki, K., Kurooka, M., Chen, J. J., Petryniak, J., Nabel, E. G., and Nabel, G. J. (2001) Extracellular matrix interacts with soluble CD95L. Retention and enhancement of cytotoxicity. Nat. Immunol. 2, 333-337 (Pubitemid 33706344)
16. Guicciardi, M. E., and Gores, G. J. (2009) Life and death by death receptors. FASEB J. 23, 1625-1637
17. Schütze, S., Tchikov, V., and Schneider-Brachert, W. (2008) Regulation of TNFR1 and CD95 signaling by receptor compartmentalization. Nat. Rev. Mol. Cell Biol. 9, 655-662 (Pubitemid 352032925)
18. Henkler, F., Behrle, E., Dennehy, K. M., Wicovsky, A., Peters, N., Warnke, C., Pfizenmaier, K., and Wajant, H. (2005) The extracellular domains of FasL and Fas are sufficient for the formation of supramolecular FasL-Fas clusters of high stability. J. Cell Biol. 168, 1087-1098
19. Siegel, R. M., Muppidi, J. R., Sarker, M., Lobito, A., Jen, M., Martin, D., Straus, S. E., and Lenardo, M. J. (2004) SPOTS. Signaling protein oligomeric transduction structures are early mediators of death receptor-induced apoptosis at the plasma membrane. J. Cell Biol. 167, 735-744 (Pubitemid 39565153)
20. Wang, L., Yang, J. K., Kabaleeswaran, V., Rice, A. J., Cruz, A. C., Park, A. Y., Yin, Q., Damko, E., Jang, S. B., Raunser, S., Robinson, C. V., Siegel, R. M., Walz, T., and Wu, H. (2010) The Fas-FADD death domain complex structure reveals the basis of DISC assembly and disease mutations. Nat. Struct. Mol. Biol. 17, 1324-1329
21. Eramo, A., Sargiacomo, M., Ricci-Vitiani, L., Todaro, M., Stassi, G., Messina, C. G., Parolini, I., Lotti, F., Sette, G., Peschle, C., and De Maria, R. (2004) CD95 death-inducing signaling complex formation and internalization occur in lipid rafts of type I and type II cells. Eur. J. Immunol. 34, 1930-1940 (Pubitemid 39256074)
22. Gajate, C., and Mollinedo, F. (2001) The antitumor ether lipid ET-18-OCH(3) induces apoptosis through translocation and capping of Fas/CD95 into membrane rafts in human leukemic cells. Blood 98, 3860-3863
23. Grassmé, H., Cremesti, A., Kolesnick, R., and Gulbins, E. (2003) Ceramide-mediated clustering is required for CD95-DISC formation. Oncogene 22, 5457-5470 (Pubitemid 37072201)
24. Grassme, H., Jekle, A., Riehle, A., Schwarz, H., Berger, J., Sandhoff, K., Kolesnick, R., and Gulbins, E. (2001) CD95 signaling via ceramide-rich membrane rafts. J. Biol. Chem. 276, 20589-20596
25. Grassmé, H., Schwarz, H., and Gulbins, E. (2001) Molecular mechanisms of ceramide-mediated CD95 clustering. Biochem. Biophys. Res. Commun. 284, 1016-1030 (Pubitemid 32924751)
26. Chakrabandhu, K., Hérincs, Z., Huault, S., Dost, B., Peng, L., Conchonaud, F., Marguet, D., He, H. T., and Hueber, A. O. (2007) Palmitoylation is required for efficient Fas cell death signaling. EMBO J. 26, 209-220 (Pubitemid 46094712)
27. Feig, C., Tchikov, V., Schütze, S., and Peter, M. E. (2007) Palmitoylation of CD95 facilitates formation of SDS-stable receptor aggregates that initiate apoptosis signaling. EMBO J. 26, 221-231 (Pubitemid 46094713)
28. Rossin, A., Kral, R., Lounnas, N., Chakrabandhu, K., Mailfert, S., Marguet, D., and Hueber, A. O. (2010) Identification of a lysine-rich region of Fas as a raft nanodomain targeting signal necessary for Fas-mediated cell death. Exp. Cell Res. 316, 1513-1522
29. Algeciras-Schimnich, A., Shen, L., Barnhart, B. C., Murmann, A. E., Burkhardt, J. K., and Peter, M. E. (2002) Molecular ordering of the initial signaling events of CD95. Mol. Cell. Biol. 22, 207-220 (Pubitemid 33144269)
30. Lee, K. H., Feig, C., Tchikov, V., Schickel, R., Hallas, C., Schütze, S., Peter, M. E., and Chan, A. C. (2006) The role of receptor internalization in CD95 signaling. EMBO J. 25, 1009-1023 (Pubitemid 43372115)
31. Parlato, S., Giammarioli, A. M., Logozzi, M., Lozupone, F., Matarrese, P., Luciani, F., Falchi, M., Malorni, W., and Fais, S. (2000) CD95 (APO-1/Fas) linkage to the actin cytoskeleton through ezrin in human T lymphocytes. A novel regulatory mechanism of the CD95 apoptotic pathway. EMBO J. 19, 5123-5134
32. Janssen, O., Lengl-Janssen, B., Oberg, H. H., Robertson, M. J., and Kabelitz, D. (1996) Induction of cell death via Fas (CD95, Apo-1) may be associated with, but is not dependent on Fas-induced tyrosine phosphorylation. Immunol Lett. 49, 63-69
33. Haake, A. R., and Polakowska, R. R. (1995) UV-induced apoptosis in skin equivalents. Inhibition by phorbol ester and Bcl-2 overexpression. Cell Death Differ. 2, 183-193
34. Siegmund, D., Wicovsky, A., Schmitz, I., Schulze-Osthoff, K., Kreuz, S., Leverkus, M., Dittrich-Breiholz, O., Kracht, M., and Wajant, H. (2005) Death receptor-induced signaling pathways are differentially regulated by γ interferon upstream of caspase 8 processing. Mol. Cell. Biol. 25, 6363-6379 (Pubitemid 41023214)
35. Wajant, H., Gerspach, J., and Pfizenmaier, K. (2011) Cancer Lett., in press
36. Tannous, B. A., Kim, D. E., Fernandez, J. L., Weissleder, R., and Breakefield, X. O. (2005) Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol. Ther. 11, 435-443 (Pubitemid 40277320)
37. Berg, D., Lehne, M., Müller, N., Siegmund, D., Münkel, S., Sebald, W., Pfizenmaier, K., and Wajant, H. (2007) Enforced covalent trimerization increases the activity of the TNF ligand family members TRAIL and CD95L. Cell Death Differ. 14, 2021-2034 (Pubitemid 350131152)
38. Wyzgol, A., Müller, N., Fick, A., Munkel, S., Grigoleit, G. U., Pfizenmaier, K., and Wajant, H. (2009) Trimer stabilization, oligomerization, and antibody-mediated cell surface immobilization improve the activity of soluble trimers of CD27L, CD40L, 41BBL, and glucocorticoid-induced TNF receptor ligand. J. Immunol. 183, 1851-1861
39. Barnhart, B. C., Alappat, E. C., and Peter, M. E. (2003) The CD95 type I/type II model. Semin. Immunol. 15, 185-193 (Pubitemid 38155825)
40. Hao, Z., and Mak, T. W. (2010) Type I and type II pathways of Fas-mediated apoptosis are differentially controlled by XIAP. J Mol. Cell. Biol. 2, 63-64
41. Martin, D. A., Zheng, L., Siegel, R. M., Huang, B., Fisher, G. H., Wang, J., Jackson, C. E., Puck, J. M., Dale, J., Straus, S. E., Peter, M. E., Krammer, P. H., Fesik, S., and Lenardo, M. J. (1999) Defective CD95/APO-1/Fas signal complex formation in the human autoimmune lymphoproliferative syndrome, type Ia. Proc. Natl. Acad. Sci. U.S.A. 96, 4552-4557 (Pubitemid 29190374)
42. Bossen, C., Ingold, K., Tardivel, A., Bodmer, J. L., Gaide, O., Hertig, S., Ambrose, C., Tschopp, J., and Schneider, P. (2006) Interactions of tumor necrosis factor (TNF) and TNF receptor family members in the mouse and human. J. Biol. Chem. 281, 13964-13971 (Pubitemid 43848322)
43. Fulda, S., Meyer, E., and Debatin, K. M. (2000) Metabolic inhibitors sensitize for CD95 (APO-1/Fas)-induced apoptosis by down-regulating Fasassociated death domain-like interleukin 1-converting enzyme inhibitory protein expression. Cancer Res. 60, 3947-3956 (Pubitemid 32204591)
44. Imanishi, T., Hano, T., Nishio, I., Liles, W. C., Schwartz, S. M., and Han, D. K. (2000) Transition of apoptotic-resistant vascular smooth muscle cells to troptotic sensitive state is correlated with down-regulation of c-FLIP. J. Vasc. Res. 37, 523-531 (Pubitemid 32037627)
45. Kreuz, S., Siegmund, D., Scheurich, P., and Wajant, H. (2001) NF-κB inducers up-regulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol. Cell. Biol. 21, 3964-3973 (Pubitemid 32476458)
46. Siegmund, D., Hadwiger, P., Pfizenmaier, K., Vornlocher, H. P., and Wajant, H. (2002) Selective inhibition of FLICE-like inhibitory protein expression with small interfering RNA oligonucleotides is sufficient to sensitize tumor cells for TRAIL-induced apoptosis. Mol. Med. 8, 725-732 (Pubitemid 36337499)
47. Papoff, G., Hausler, P., Eramo, A., Pagano, M. G., Di Leve, G., Signore, A., and Ruberti, G. (1999) Identification and characterization of a ligandin-dependent oligomerization domain in the extracellular region of the CD95 death receptor. J. Biol. Chem. 274, 38241-38250 (Pubitemid 30026900)
48. Siegel, R. M., Frederiksen, J. K., Zacharias, D. A., Chan, F. K., Johnson, M., Lynch, D., Tsien, R. Y., and Lenardo, M. J. (2000) Fas preassociation required for apoptosis signaling and dominant inhibition by pathogenic mutations. Science 288, 2354-2357 (Pubitemid 30448157)
49. Kischkel, F. C., Hellbardt, S., Behrmann, I., Germer, M., Pawlita, M., Krammer, P. H., and 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
50. Esposito, D., Sankar, A., Morgner, N., Robinson, C. V., Rittinger, K., and Driscoll, P. C. (2010) Solution NMR investigation of the CD95/FADD homotypic death domain complex suggests a lack of engagement of the CD95 C terminus. Structure 18, 1378-1390
51. Kleber, S., Sancho-Martinez, I., Wiestler, B., Beisel, A., Gieffers, C., Hill, O., Thiemann, M., Mueller, W., Sykora, J., Kuhn, A., Schreglmann, N., Letellier, E., Zuliani, C., Klussmann, S., Teodorczyk, M., Gröne, H. J., Ganten, T. M., Sültmann, H., Tüttenberg, J., von Deimling, A., Regnier- Vigouroux, A., Herold-Mende, C., and Martin-Villalba, A. (2008) Yes and PI3K bind CD95 to signal invasion of glioblastoma. Cancer Cell 13, 235-248 (Pubitemid 351324880)
52. Tauzin, S., Chaigne-Delalande, B., Selva, E., Khadra, N., Daburon, S., Contin-Bordes, C., Blanco, P., Le Seyec, J., Ducret, T., Counillon, L., Moreau, J. F., Hofman, P., Vacher, P., and Legembre, P. (2011) The naturally processed CD95L elicits a c-yes/calcium/PI3K-driven cell migration pathway. PLoS Biol. 9, e1001090
53. O' Reilly, L.A., Tai, L., Lee, L., Kruse, E. A., Grabow, S., Fairlie, W. D., Haynes, N. M., Tarlinton, D. M., Zhang, J. G., Belz, G. T., Smyth, M. J., Bouillet, P., Robb, L., and Strasser, A. (2009) Membrane-bound Fas ligand only is essential for Fas-induced apoptosis. Nature 461, 659-663
54. Roos, C., Wicovsky, A., Müller, N., Salzmann, S., Rosenthal, T., Kalthoff, H., Trauzold, A., Seher, A., Henkler, F., Kneitz, C., and Wajant, H. (2010) Soluble and transmembrane TNF-like weak inducer of apoptosis differentially activates the classical and noncanonical NF-κ B pathway. J. Immunol. 185, 1593-1605
55. Aggarwal, B. B., Eessalu, T. E., and Hass, P. E. (1985) Characterization of receptors for human tumornecrosis factor and their regulation by γ-interferon. Nature 318, 665-667 (Pubitemid 16172416)
56. Baglioni, C., McCandless, S., Tavernier, J., and Fiers, W. (1985) Binding of human tumor necrosis factor to high affinity receptors on HeLa and lymphoblastoid cells sensitive to growth inhibition. J. Biol. Chem. 260, 13395-13397 (Pubitemid 16192281)
57. Grell, M., Wajant, H., Zimmermann, G., and Scheurich, P. (1998) The type 1 receptor (CD120a) is the high affinity receptor for soluble tumor necrosis factor. Proc. Natl. Acad. Sci. U.S.A. 95, 570-575 (Pubitemid 28083784)
58. Smith, R. A., and Baglioni, C. (1987) The active form of tumor necrosis factor is a trimer. J. Biol. Chem. 262, 6951-6954 (Pubitemid 17105009)
59. Bentele, M., Lavrik, I., Ulrich, M., Stösser, S., Heermann, D. W., Kalthoff, H., Krammer, P. H., and Eils, R. (2004) Mathematical modeling reveals threshold mechanism in CD95-induced apoptosis. J. Cell Biol. 166, 839-851 (Pubitemid 39249835)
60. Lavrik, I. N., Golks, A., Riess, D., Bentele, M., Eils, R., and Krammer, P. H. (2007) Analysis of CD95 threshold signaling. Triggering of CD95 (FAS/ APO-1) at low concentrations primarily results in survival signaling. J. Biol. Chem. 282, 13664-13671 (Pubitemid 47100557)
61. Faubion, W. A., Guicciardi, M. E., Miyoshi, H., Bronk, S. F., Roberts, P. J., Svingen, P. A., Kaufmann, S. H., and Gores, G. J. (1999) Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J. Clin. Invest. 103, 137-145 (Pubitemid 29031172)
62. Fumarola, C., Zerbini, A., and Guidotti, G. G. (2001) Glutamine deprivation-mediated cell shrinkage induces ligand-independent CD95 receptor signaling and apoptosis. Cell Death Differ. 8, 1004-1013 (Pubitemid 32994651)
63. Gajate, C., Fonteriz, R. I., Cabaner, C., Alvarez-Noves, G., Alvarez-Rodriguez, Y., Modolell, M., and Mollinedo, F. (2000) Intracellular triggering of Fas, independently of FasL, as a new mechanism of antitumor ether lipid-induced apoptosis. Int. J. Cancer 85, 674-682 (Pubitemid 30080481)
64. Micheau, O., Solary, E., Hammann, A., and Dimanche-Boitrel, M. T. (1999) Fas ligand-independent, FADD-mediated activation of the Fas death pathway by anticancer drugs. J. Biol. Chem. 274, 7987-7992