Inhibition of NF-κB activity in human T lymphocytes induces caspase- dependent apoptosis without detectable activation of caspase-1 and -3

Journal of Immunology

Volumn 163, Issue 2, 1999, Pages 590-598

  Kolenko, Vladimir ^a   Bloom, Tracy ^a   Rayman, Patricia ^a   Bukowski, Ronald ^a   Hsi, Eric ^a   Finke, James ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 3; CASPASE INHIBITOR; FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; N,N,N',N' TETRAKIS(2 PYRIDYLMETHYL)ETHYLENEDIAMINE; PEPTIDE; PHOSPHATIDYLSERINE;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; T LYMPHOCYTE; TRANSCRIPTION REGULATION;

APOPTOSIS; CASPASE 1; CASPASE 3; CASPASE 6; CASPASES; CELL SURVIVAL; ENZYME ACTIVATION; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INTERPHASE; LYMPHOCYTE ACTIVATION; NF-KAPPA B; PEPTIDES; PHOSPHATIDYLSERINES; PROTEIN BINDING; T-LYMPHOCYTES;

EID: 0033565406     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Baeuerle, P. A., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:141.
2. Baeuerle, P. A., and D. Baltimore. 1996. NF-κB: ten years after. Cell 87:13.
3. Molitor, J. A., W. H. Walker, D. Doerre, D. W. Ballard, and W. C. Greene. 1990. NF-κB: a family of inducible and differentially expressed enhancer-binding proteins in human T cells. Proc. Natl. Acad. Sci. USA 87:10028.
4. Arima, N., W. A. Kuziel, T. A. Grdina, and W. C. Greene. 1992. IL-2-induced signal transduction involves the activation of nuclear NF-κB expression. J. Immunol. 149:83.
5. Granelli-Piperno, A., and P. Nolon. 1991. Nuclear transcription factors that bind to elements of the IL-2 promoter: induction requirements in primary human T cells. J. Immunol. 147:2734.
6. Costello, R., C. Lipcey, M. Algarte, C. Cerdan, P. A. Baeuerle, D. Olive, and J. Imbert. 1993. Activation of primary human T-lymphocytes through CD2 plus CD28 adhesion molecules induces long-term nuclear expression of NF-κB. Cell Growth Differ. 4:329.
7. Lowenthal, J. W., D. W. Ballard, E. Bohnlein, and W. C. Greene. 1989. Tumor necrosis factor a induces proteins that bind specifically to κB-like enhancer elements and regulate interleukin-2 receptor α-chain gene expression in primary human T lymphocytes. Proc. Natl. Acad. Sci. USA 86:2331.
8. Beg, A. A., T. S. Finco, P. V. Nantermet, and A. S. Baldwin, Jr. 1993. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκBα: a mechanism for NF-κB activation. Mol. Cell. Biol. 13:3301.
9. Palombella, V., O. Rando, A. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell 78:773.
10. Brown, K., S. Gerstberger, L. Carlson, G. Franzoso, and U. Siebenlist. 1995. Control of IκB-α proteolysis by site-specific, signal-induced phosphorylation. Science 267:1485.
11. Thompson, J. E., R. J. Phillips, H. Erdjumant-Bromage, P. Tempst, and S. Ghosh. 1995. IκB-β regulated the persistent response in a biphasic activation of NF-κB. Cell 80:573.
12. Brockman, J. A., D. C. Scherer, T. A. McKinsey, S. M. Hall, X. Qi, W. Y. Lee, and D. W. Ballard. 1995. Coupling of signal response domain in IκBα to multiple pathways for NF-κB activation. Mol. Cell. Biol. 15: 2809.
13. Traenckner, E. B., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human IκBα on serines 32 and 36 controls IκBα proteolysis and NF-κB activation in response to diverse stimuli. EMBO J. 14:2876.
14. La Rosa, F. A., J. P. Pierce, and G. E. Sonenshein. 1994. Differential regulation of the c-myc oncogene promoter by the NF-κB rel family of transcription factors. Mol. Cell. Biol. 14:1039.
15. Wu, H., and G. Lozano. 1994. NF-κB activation of p53. A potential mechanism for suppressing cell growth in response to stress. J. Biol. Chem. 269:20067.
16. Beg, A. A., W. Sha, R. Bronson, S. Ghosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the ReIA component of NF-κB. Nature 376:167.
17. Wang, C.-Y., M. W. Mayo, and A. S. Baldwin, Jr. 1996. TNF- and cancer therapy induced apoptosis: potentiation by inhibition of NF-κB. Science 274:784.
18. Wu, M., H. Lee, R. E. Bellas, S. L. Schauer, M. Arsura, D. Katz, M. J. FitzGerald, T. L. Rothstein, D. H. Sherr, and G. E. Sonenshein. 1996. Inhibition of NF-κB/ Rel induces apoptosis of murine B cells. EMBO J. 15:4682.
19. Arsura, M., M. Wu, and G. E. Sonenshein. 1996. TGFβ1 inhibits NF-κB/Rel activity inducing apoptosis of B cells: transcriptional activation of IκB-α. Immunity 5:31.
20. Ravi, R., A. Bedi, E. J. Fuchs, and A. Bedi. 1998. CD95 (Fas)-induced caspase-mediated proteolysis of NF-κB. Cancer Res. 58:882.
21. Alnemri, E. S., D. J. Livingston, D. W. Nicholson, G. Salvesen, N. A. Thornberry, W. W. Wong, and J. Yuan. 1996. Human ICE/CED-3 protease nomenclature. Cell 87:171.
22. Chinnaiyan, A. M., K. Orth, K. O'Rourke, H. Duan, G. G. Poirier, and V. M. Dixit. 1996. Molecular ordering of cell death pathway. J. Biol. Chem. 271:4573.
23. Orth, K., K. O'Rourke, G. S. Salvesen, and V. M. Dixit. 1996. Molecular ordering of apoptotic mammalian CED-3/ICE-like proteases. J. Biol. Chem. 271:20977.
24. Enari, M., R. V. Talanian, W. W. Wong, and S. Nagata. 1996. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380:723.
25. Salvesen, G. S., and V. M. Dixit. 1997. Caspases: intracellular signaling by proteolysis. Cell 91:443.
26. Nagata, S. 1997. Apoptosis by death factor. Cell 88:355.
27. Martin, S. J., D. D. Newmeyer, S. Mathias, D. M. Farschon, H.-G. Wang, J. C. Reed, R. N. Kolesnic, and D. R. Green. 1995. Cell-free reconstitution of Fas-, UV radiation and ceramide-induced apoptosis. EMBO J. 14:5191.
28. Fraser, A., and G. Evan. 1996. A license to kill. Cell 85:781.
29. Takahashi, A., and W. C. Earnshaw. 1996. ICE-related proteases in apoptosis. Curr. Opin. Genet. Dev. 6:50.
30. Nava, V. E., A. Rosen, M. A. Veliuona, R. J. Clem, B. Levine, and J. M. Hardwick. 1998. Sindbis virus induces apoptosis through a caspase-dependent, CrmA-sensitive pathway. J. Virol. 72:452.
31. Nicholson, D. W., A. Ali, N. A. Thornberry, J. P. Vaillancourt, C. K. Ding, M. Gallant, Y. Gareau, P. R. Griffin, M. Labelle, and Y. A. Lazebnik. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376:37.
32. Tewari, M., L. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D. R. Beidler, G. G. Poirier, G. S. Salvesen, and V. M. Dixit. 1995. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:801.
33. An, B., J. R. Jin, P. Lin, and Q. P. Dou. 1996. Failure to activate interleukin-1β converting enzyme like proteases and to cleave retinoblastoma protein in drug-resistant cells. FEBS Lett. 399:158.
34. Janicke, R. U., P. A. Walker, X. Y. Lin, and A. G. Porter. 1996. Specific cleavage of the retinoblastoma protein by an ICE-like protease in apoptosis. EMBO J. 15:6969.
35. Martin, S. J., G. A. O'Brien, W. K. Nishioka, A. J. McGahon, A. Mahboubi, T. C. Saido, and D. R. Green. 1995. Proteolysis of fodrin (non-erythroid spectrin) during apoptosis. J. Biol. Chem. 270:6425.
36. Cryns, V. L., H. Bergeron, H. Zhu, J. Li, and J. Yuan. 1996. Specific cleavage of α-fodrin during Fas- and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1β-converting enzyme/Ced-3 protease distinct from the poly-(ADP-ribose) polymerase protease. J. Biol. Chem. 271:31277.
37. Lazebnik, Y. A., A. Takahashi, R. D. Moir, R. D. Goldman, G. G. Poirier, S. H. Kaufmann, and W. C. Earnshaw. 1995. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad Sci. USA 92:9042.
38. Rao, L., D. Perez, and E. White. 1996. Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135:1441.
39. Cheng, E. H., D. G. Kirsch, R. J. Clem, R. Ravi, M. B. Kastan, A. Bedi, K. Ueno, and J. M. Hardwick. 1997. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278:1966.
40. L through caspase interaction. Proc. Natl. Acad. Sci. USA 95:554.
41. Liu, X., H. Zou, C. Slaughter, and H. Wang. 1997. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89:175.
42. Jeremias, I., C. Kupatt, B. Baumann, I. Herr, T. Wirth, and K. M. Debatin. 1998. Inhibition of nuclear factor κB activation attenuates apoptosis resistance in lymphoid cells. Blood 91:4624.
43. Lin, Y. Z., S. Y. Yao, R. A. Veach, T. R. Torgerson, and J. Hawiger. 1995. Inhibition of nuclear translocation of transcription factor NF-κB by a synthetic peptide containing a cell membrane-permeable motif and nuclear lacalization sequence. J. Biol. Chem. 270:14255.
44. lck in T-cell infiltrating human renal cell carcinoma. Cancer Res. 53:5613.
45. Wang, Q., J. Stanley, S. Kudoh, J. Myles, V. M. Kolenko, T. Yi, R. R. Tubbs, R. M. Bukowski, and J. H. Finke. 1995. T Cells infiltrating non-Hodgkin's B cell lymphomas show altered tyrosine phosphorylation pattern even though T cell receptor/CD3-associated kinases are present. J. Immunol. 155:1382.
46. Kolenko, V., Q. Wang, M. C. Riedy, J. O'Shea, J. Ritz,. M. K. Cathcart, P. Rayman, R. Tubbs, M. Edinger, A. Novick, R. Bukowski, and J. Finke. 1997. Tumor-induced suppression of T lymphocyte proliferation coincides with inhibition of Jak3 expression and IL-2 receptor signaling: role of soluble products from human renal cell carcinomas. J. Immunol. 159:3057.
47. Koopman, G., C. P. M. Reutelingsperger, G. A. M. Kuijten, R. M. J. Keehnen, S. T. Pals, and M. H. J. Oers. 1994. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84:1415.
48. Zamzami, N., P. Marchetti, M. Castedo, C. Zanin, J.-L. Vayssiere, P. X. Petit, and G. Kroemer. 1995. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1661.
49. Torgerson, T., A. D. Colosia, J. P. Donahue, Y.-Z. Lin, and J. Hawiger. 1998. Regulation of NF-κB, AP-1, NFAT, and STAT1 nuclear import in T lymphocytes by noninvasive delivery of peptide carrying the nuclear localization sequence of NF-κB p50. J. Immunol. 161:6084.
50. Treves, S., P. L. Trentini, M. Ascanelli, G. Bucci, and F. DiVirgilio. 1994. Apoptosis is dependent on intracellular zinc and independent on intracellular calcium in lymphocytes. Exp. Cell Res. 211:339.
51. Fadok, V. A., D. R. Voelker, P. A. Campbell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207.
52. Fadok, V. A., J. S. Savill, S. Haslett, D. L. Bratton, D. E. Doherty, P. A. Campbell, and P. M. Henson. 1992. Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J. Immunol. 149:4029.
53. Martin, S. J., C. P. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. van Schie, D. M. LaFace, and D. R. Green. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Ab1. J. Exp. Med. 182:1545.
54. Martin, S. J., D. M. Finucane, G. P. Amarante-Mendes, G. A. O'Brien, and D. R. Green. 1996. Phosphatidylserine externalization during CD95-induced apoptosis of cells and cytoplasts requires ICE/CED-3 protease activity. J. Biol. Chem. 271:28753.
55. Garsia-Calvo, M., E. P. Peterson, B. Leiting, R. Ruel, D. W. Nicholson, and N. A. Thornberry. 1998. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J. Biol. Chem. 273:32608.
56. L. Immunity 3:87.
57. S) gene expression. Eur. J. Immunol. 26:294.
58. Broome, H. E., C. M. Dargan, S. Krajewski, and J. C. Reed. 1995. Expression of Bcl-2, Bcl-x, and Bax after T cell activation and IL-2 withdrawal. J. Immunol. 155:2311.
59. Pierce, J. W., R. Schoenleber, G. Jesmok, J. Best, S. A. Moore, T. Collins, and M. E. Gerritsen. 1997. Novel inhibitors of cytokine-induced IκBα phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J. Biol. Chem. 272:21096.
60. Ling, W., P. Rayman, R. Uzzo, P. Clark, H. J. Kim, R. Tubbs, A. Novick, R. Bukowski, T. Hamilton, and J. Finke. 1998. Impaired activation of NF-κB in T cells from a subset of renal cell carcinoma patients is mediated by inhibition of phosphorylation and degradation of the inhibitor, IκBα. Blood 92:1.
61. Correa, M. R., A. C. Ochoa, P. Ghosh, H. Mizoguchi, L. Harvey, and D. L. Longo. 1997. Sequential development of structural and functional alterations in T cells from tumor-bearing mice. J. Immunol. 158:5292.
62. Romano, M. F., A. Lamberti, A. Petrella, R. Bisogni, P. F. Tassone, S. Formisano, S. Venuta, and M. C. Turco. 1996. IL-10 inhibits nuclear factor-κ B/Rel nuclear activity in CD3-stimulated human peripheral T lymphocytes. J. Immunol. 156:2119.
63. Chen, D., and E. V. Rothenberg. 1994. Interleukin 2 transcription factors as molecular targets of cAMP inhibition: delayed inhibition kinetics and combinatorial transcription roles. J. Exp. Med. 179:931.
64. Irani, D. N., K. I. Lin, and D. E. Griffin. 1996. Brain-derived gangliosides regulate the cytokine production and proliferation of activated T cells. J. Immunol. 157:4333.