A Fas-associated death domain protein/caspase-8-signaling axis promotes S-phase entry and maintains S6 kinase activity in T cells responding to IL-2 1

Journal of Immunology

Volumn 179, Issue 8, 2007, Pages 5291-5300

  Arechiga, Adrian F ^a,d   Bell, Bryan D ^a   Leverrier, Sabrina ^a   Weist, Brian M ^a   Porter, Melissa ^b   Wu, Zhengqi ^b   Kanno, Yuka ^b   Ramos, Stephanie J ^a   Ong, S Tiong ^c   Siegel, Richard ^b   Walsh, Craig M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; CYCLIN D3; CYCLIN DEPENDENT KINASE 2; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FLICE INHIBITORY PROTEIN; INITIATION FACTOR 4E BINDING PROTEIN 1; INTERLEUKIN 2; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN S6; RETINOBLASTOMA PROTEIN; S6 KINASE; S6 KINASE 1; SERINE; UNCLASSIFIED DRUG; VIRUS PROTEIN; CASP8 PROTEIN, MOUSE; FADD PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; ENZYMOLOGY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

ANIMALS; CASPASE 8; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 2; ENZYME ACTIVATION; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; HUMANS; INTERLEUKIN-2; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHORYLATION; RIBOSOMAL PROTEIN S6 KINASES; S PHASE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

EID: 38449096218     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.8.5291     Document Type: Article

References (68)

1. Chinnaiyan, A. M., K. O'Rourke, M. Tewari, and V. M. Dixit. 1995. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81: 505-512.
2. Boldin, M., E. Varfolomeev, Z. Pancer, I. Mett, J. Camonis, and D. Wallach. 1995. 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: 7795-7798.
3. Hsu, H., J. Xiong, and D. V. Goeddel. 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-κB activation. Cell 81: 495-504.
4. Eberstadt, M., B. Huang, Z. Chen, R. P. Meadows, S. C. Ng, L. Zheng, M. J. Lenardo, and S. W. Fesik. 1998. NMR structure and mutagenesis of the FADD (Mort1) death-effector domain. Nature 392: 941-945.
5. Hsu, H., H. Shu, M. Pan, and D. Goeddel. 1996. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84: 299-308.
6. Ashkenazi, A., and V. Dixit. 1998. Death receptors: signaling and modulation. Science 281: 1305-1308.
7. Muzio, M., B. R. Stockwell, H. R. Stennicke, G. S. Salvesen, and V. M. Dixit. 1998. An induced proximity model for caspase-8 activation. J. Biol. Chem. 273: 2926-2930.
8. MacCorkle, R. A., K. W. Freeman, and D. M. Spencer. 1998. Synthetic activation of caspases: artificial death switches. Proc. Natl. Acad. Sci. USA 95: 3655-3660.
9. Siegel, R. M., J. R. Muppidi, M. Sarker, A. Lobito, M. Jen, D. Martin, S. E. Straus, and M. J. Lenardo. 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.
10. Muppidi, J. R., A. A. Lobito, M. Ramaswamy, J. K. Yang, L. Wang, H. Wu, and R. M. Siegel. 2006. Homotypic FADD interactions through a conserved RXDLL motif are required for death receptor-induced apoptosis. Cell Death Differ. 13: 1641-1650.
11. Sandu, C., G. Morisawa, I. Wegorzewska, T. Huang, A. F. Arechiga, J. M. Hill, T. Kim, C. M. Walsh, and M. H. Werner. 2006. FADD self-association is required for stable interaction with an activated death receptor. Cell Death Differ. 13: 2052-2061.
12. Walsh, C. M., K. A. Luhrs, and A. F. Arechiga. 2003. The "fuzzy logic" of the death-inducing signaling complex in lymphocytes. J. Clin. Immunol. 23: 333-353.
13. Werner, M. H., C. Wu, and C. M. Walsh. 2006. Emerging roles for the death adaptor FADD in death receptor avidity and cell cycle regulation. Cell Cycle 5: 2332-2338.
14. Zhang, J., D. Cado, A. Chen, N. Kabra, and A. Winoto. 1998. Fas-mediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/Mort1. Nature 392: 296-300.
15. Newton, K., A. Harris, M. Bath, K. Smith, and A. Strasser. 1998. A dominant interfering mutant of FADD/MORT1 enhances deletion of autoreactive thymocytes and inhibits proliferation of mature T lymphocytes. EMBO J. 17: 706 -718.
16. Walsh, C., B. Wen, A. Chinnaiyan, K. O'Rourke, V. Dixit, and S. Hedrick. 1998. A role for FADD in T cell activation and development. Immunity 8: 439-449.
17. Hueber, A. O., M. Zornig, A. M. Bernard, M. Chautan, and G. Evan. 2000. A dominant negative Fas-associated death domain protein mutant inhibits proliferation and leads to impaired calcium mobilization in both T-cells and fibroblasts. J. Biol. Chem. 275: 10453-10462.
18. Kabra, N. H., C. Kang, L. C. Hsing, J. Zhang, and A. Winoto. 2001. T cell-specific FADD-deficient mice: FADD is required for early T cell development. Proc. Natl. Acad. Sci. USA 98: 6307-6312.
19. Zhang, J., N. H. Kabra, D. Cado, C. Kang, and A. Winoto. 2001. FADD-deficient T cells exhibit a disaccord in regulation of the cell cycle machinery. J. Biol. Chem. 276: 29815-29818.
20. Newton, K., C. Kurts, A. W. Harris, and A. Strasser. 2001. Effects of a dominant interfering mutant of FADD on signal transduction in activated T cells. Curr. Biol. 11: 273-276.
21. Beisner, D. R., I. H. Chu, A. F. Arechiga, S. M. Hedrick, and C. M. Walsh. 2003. The requirements for Fas-associated death domain signaling in mature T cell activation and survival. J. Immunol. 171: 247-256.
22. Chun, H. J., L. Zheng, M. Ahmad, J. Wang, C. K. Speirs, R. M. Siegel, J. K. Dale, J. Puck, J. Davis, C. G. Hall, et al. 2002. Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature 419: 395-399.
23. Su, H., N. Bidere, L. Zheng, A. Cubre, K. Sakai, J. Dale, L. Salmena, R. Hakem, S. Straus, and M. Lenardo. 2005. Requirement for caspase-8 in NF-κB activation by antigen receptor. Science 307: 1465-1468.
24. Arechiga, A. F., B. D. Bell, J. C. Solomon, I. H. Chu, C. L. Dubois, B. E. Hall, T. C. George, D. M. Coder, and C. M. Walsh. 2005. Cutting edge: FADD is not required for antigen receptor-mediated NF-κB activation. J. Immunol. 175: 7800-7804.
25. Nelson, B. H., and D. M. Willerford. 1998. Biology of the interleukin-2 receptor. Adv. Immunol. 70: 1-81.
26. Van Parijs, L., Y. Refaeli, J. D. Lord, B. H. Nelson, A. K. Abbas, and D. Baltimore. 1999. Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation-induced cell death. Immunity 11: 281-288.
27. Refaeli, Y., L. Van Parijs, C. A. London, J. Tschopp, and A. K. Abbas. 1998. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 8: 615-623.
28. + T cell memory. J. Immunol. 172: 6313-6323.
29. Kennedy, N. J., T. Kataoka, J. Tschopp, and R. C. Budd. 1999. Caspase activation is required for T cell proliferation. J. Exp. Med. 190: 1891-1896.
30. Alam, A., L. Y. Cohen, S. Aouad, and R. P. Sekaly. 1999. Early activation of caspases during T lymphocyte stimulation results in selective substrate cleavage in nonapoptotic cells. J. Exp. Med. 190: 1879-1890.
31. Mack, A., and G. Hacker. 2002. Inhibition of caspase or FADD function blocks proliferation but not MAP kinase-activation and interleukin-2-production during primary stimulation of T cells. Eur. J. Immunol. 32: 1986-1992.
32. Beisner, D. R., I. L. Ch'en, R. V. Kolla, A. Hoffmann, and S. M. Hedrick. 2005. Cutting edge: innate immunity conferred by B cells is regulated by caspase-8. J. Immunol. 175: 3469-3473.
33. Pesu, M., L. Muul, Y. Kanno, and J. J. O'Shea. 2006. Proprotein convertase furin is preferentially expressed in T helper 1 cells and regulates interferon γ. Blood 108: 983-985.
34. Deane, J. A., and D. A. Fruman. 2004. Phosphoinositide 3-kinase: diverse roles in immune cell activation. Annu. Rev. Immunol. 22: 563-598.
35. Manning, B. D., A. R. Tee, M. N. Logsdon, J. Blenis, and L. C. Cantley. 2002. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell. 10: 151-162.
36. Astoul, E., A. D. Laurence, N. Totty, S. Beer, D. R. Alexander, and D. A. Cantrell. 2003. Approaches to define antigen receptor-induced serine kinase signal transduction pathways. J. Biol. Chem. 278: 9267-9275.
37. Obata, T., M. B. Yaffe, G. G. Leparc, E. T. Piro, H. Maegawa, A. Kashiwagi, R. Kikkawa, and L. C. Cantley. 2000. Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J. Biol. Chem. 275: 36108-36115.
38. Zhang, H., X. Zha, Y. Tan, P. V. Hornbeck, A. J. Mastrangelo, D. R. Alessi, R. D. Polakiewicz, and M. J. Comb. 2002. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 277: 39379-39387.
39. Ly, C., A. F. Arechiga, J. V. Melo, C. M. Walsh, and S. T. Ong. 2003. Bcr-Abl kinase modulates the translation regulators ribosomal protein S6 and 4E-BP1 in chronic myelogenous leukemia cells via the mammalian target of rapamycin. Cancer Res. 63: 5716-5722.
40. Dufner, A., and G. Thomas. 1999. Ribosomal S6 kinase signaling and the control of translation. Exp. Cell Res. 253: 100-109.
41. Romanelli, A., V. C. Dreisbach, and J. Blenis. 2002. Characterization of phosphatidylinositol 3-kinase-dependent phosphorylation of the hydrophobic motif site Thr389 in p70 S6 kinase 1. J. Biol. Chem. 277: 40281-40289.
42. Waskiewicz, A. J., J. C. Johnson, B. Penn, M. Mahalingam, S. R. Kimball, and J. A. Cooper. 1999. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol. Cell. Biol. 19: 1871-1880.
43. Pyronnet, S., H. Imataka, A. C. Gingras, R. Fukunaga, T. Hunter, and N. Sonenberg. 1999. Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J. 18: 270-279.
44. Morgan, D. O. 1997. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13: 261-291.
45. 0→G1 that controls entry into the cell cycle. Mol. Cell. Biol. 23: 2351-2361.
46. Hleb, M., S. Murphy, E. F. Wagner, N. N. Hanna, N. Sharma, J. Park, X. C. Li, T. B. Strom, J. F. Padbury, Y. T. Tseng, and S. Sharma. 2004. Evidence for cyclin d3 as a novel target of rapamycin in human T lymphocytes. J. Biol. Chem. 279: 31948-31955.
47. 1 cell-cycle progression by oncogenes and tumor suppressor genes. Curr. Opin. Genet. Dev. 12: 47-52.
48. Pan, W., S. Cox, R. H. Hoess, and R. H. Grafstrom. 2001. A cyclin D1/cyclin-dependent kinase 4 binding site within the C domain of the retinoblastoma protein. Cancer Res. 61: 2885-2891.
49. 1 cyclin-dependent kinase complexes in vivo. Mol. Cell. Biol. 21: 4773-4784.
50. Salmena, L., B. Lemmers, A. Hakem, E. Matysiak-Zablocki, K. Murakami, P. Y. Au, D. M. Berry, L. Tamblyn, A. Shehabeldin, E. Migon, et al. 2003. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 17: 883-895.
51. Siegel, R. M. 2006. Caspases at the crossroads of immune-cell life and death. Nat. Rev. Immunol. 6: 308-317.
52. Yoshimura, A., M. Ichihara, I. Kinjyo, M. Moriyama, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, T. Hara, and A. Miyajima. 1996. Mouse oncostatin M: an immediate early gene induced by multiple cytokines through the JAK-STAT5 pathway. EMBO J. 15: 1055-1063.
53. Kim, D. H., and D. M. Sabatini. 2004. Raptor and mTOR: subunits of a nutrient-sensitive complex. Curr. Top. Microbiol. Immunol. 279: 259-270.
54. Bidere, N., A. L. Snow, K. Sakai, L. Zheng, and M. J. Lenardo. 2006. Caspase-8 regulation by direct interaction with TRAF6 in T cell receptor-induced NF-κB activation. Curr. Biol. 16: 1666-1671.
55. Fingar, D. C., S. Salama, C. Tsou, E. Harlow, and J. Blenis. 2002. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/ eIF4E. Genes Dev. 16: 1472-1487.
56. -/- mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol. Cell. Biol. 24: 3112-3124.
57. Roux, P. P., D. Shahbazian, H. Vu, M. K. Holz, M. S. Cohen, J. Taunton, N. Sonenberg, and J. Blenis. 2007. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J. Biol. Chem. 282: 14056-14064.
58. Shah, O. J., S. Ghosh, and T. Hunter. 2003. Mitotic regulation of ribosomal S6 kinase 1 involves Ser/Thr, Pro phosphorylation of consensus and non-consensus sites by Cdc2. J. Biol. Chem. 278: 16433-16442.
59. Hou, Z., L. He, and R. Z. Qi. 2007. Regulation of S6 kinase 1 activation by phosphorylation at Ser-411. J. Biol. Chem. 282: 6922-6928.
60. Sulic, S., L. Panic, M. Barkic, M. Mercep, M. Uzelac, and S. Volarevic. 2005. Inactivation of S6 ribosomal protein gene in T lymphocytes activates a p53-dependent checkpoint response. Genes Dev. 19: 3070-3082.
61. Reif, K., B. M. Burgering, and D. A. Cantrell. 1997. Phosphatidylinositol 3-kinase links the interleukin-2 receptor to protein kinase B and p70 S6 kinase. J. Biol. Chem. 272: 14426-14433.
62. Fruman, D. A., M. A. Wood, C. K. Gjertson, H. R. Katz, S. J. Burakoff, and B. E. Bierer. 1995. FK506 binding protein 12 mediates sensitivity to both FK506 and rapamycin in murine mast cells. Eur. J. Immunol. 25: 563-571.
63. Kuo, C. J., J. Chung, D. F. Fiorentino, W. M. Flanagan, J. Blenis, and G. R. Crabtree. 1992. Rapamycin selectively inhibits interleukin-2 activation of p70 S6 kinase. Nature 358: 70-73.
64. Brennan, P., J. W. Babbage, B. M. Burgering, B. Groner, K. Reif, and D. A. Cantrell. 1997. Phosphatidylinositol 3-kinase couples the interleukin-2 receptor to the cell cycle regulator E2F. Immunity 7: 679-689.
65. s6k integrates phosphatidylinositol 3-kinase and rapamycin-regulated signals for E2F regulation in T lymphocytes. Mol. Cell. Biol. 19: 4729-4738.
66. 1-S cell cycle progression of T lymphocytes. Nat. Immunol. 8: 64-73.
67. Arai, S., K. Miyake, R. Voit, S. Nemoto, E. K. Wakeland, I. Grummt, and T. Miyazaki. 2007. Death-effector domain-containing protein DEDD is an inhibitor of mitotic Cdk1/cyclin B1. Proc. Natl. Acad. Sci. USA 104: 2289-2294.
68. Klionsky, D. J., A. J. Meijer, and P. Codogno. 2005. Autophagy and p70S6 kinase. Autophagy 1: 59-60, discussion 60-61.