In vivo inhibition of NF-κB in T-lineage cells leads to a dramatic decrease in cell proliferation and cytokine production and to increased cell apoptosis in response to mitogenic stimuli, but not to abnormal thymopoiesis

Journal of Immunology

Volumn 162, Issue 11, 1999, Pages 6442-6450

  Ferreira, Valérie ^a   Sidénius, Nicolai ^b   Tarantino, Nadine ^a   Hubert, Pascale ^a   Chatenoud, Lucienne ^c   Blasi, Francesco ^b   Körner, Marie ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; MITOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL DIVISION; CYTOKINES; DNA-BINDING PROTEINS; FEMALE; HUMANS; I-KAPPA B PROTEINS; INTERFERON TYPE II; INTERLEUKIN-10; INTERLEUKIN-2; INTERLEUKIN-4; IONOMYCIN; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MITOGENS; NF-KAPPA B; RECEPTORS, INTERLEUKIN-2; T-LYMPHOCYTES; TETRADECANOYLPHORBOL ACETATE; THYMUS GLAND; TRANSGENES;

EID: 0345593715     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (72)

1. Jamieson, C., P. O. McCaffrey, A. Rao, and R. Sen. 1991. Physiologic activation of T cells via the T cell receptor induces NF-κB. J. Immunol. 147:416.
2. Sen, J., L. Venkataraman, Y. Shinkai, J. W. Pierce, F. W. Alt, S. J. Burakoff, and R. Sen. 1995. Expression and induction of nuclear factor-κB-related proteins in thymocytes. J. Immunol. 154:3213.
3. Baldwin, A. S. 1996. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649.
4. Baeuerle, P. A., T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:141.
5. Körner, M., N. Tarantino, and P. Debré. 1991. Constitutive activation of NF-κB in human thymocytes. Biochem. Biophys. Res. Commun. 181:80.
6. Feuillard, J., C. Dargemont, V. Ferreira, N. Tarantino, P. Debré, M. Raphael, and M. Körner. 1997. Nuclear Re1-A and c-Re1 ptolein complexes are differentially distributed within human thymocytes. J. Immunol. 158:2585.
7. Weih, F., D. Carrasco, and R. Bravo. 1994. Constitutive and inducible Rel/NF-κB activities in mouse thymus and spleen. Oncogene 9:3289.
8. Ivanov, V., and R. Ceredig. 1992. Transcription factors in mouse fetal thymus development. Int. Immunol. 4:729.
9. Grilli, M., J.-S. Chiu, and M. Lenardo. 1993. NF-κB and Rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143:1.
10. Beg, A. A., S. M. Ruben, R. I. Scheinman, S. Haskill, C. A. Rosen, and A. S. Baldwin. 1992. IκB interacts with the nuclear localization sequences of the subunits of NF-κB. Genes Dev. 6:1899.
11. Baeuerle, P. A., D. Baltimore. 1996. NF-κB: ten years after. Cell 87:13.
12. Beg, A. A., W. C. Sha, R. T. Bronson, and D. Baltimore. 1995. Constitutive NF-κB activation, enhanced granulopoiesis, and neonatal lethality in IκBα-deficient mice. Genes Dev. 9:2736.
13. Haskill, S., A. A. Beg, S. M. Tompkins, J. S. Morris, A. D. Yurochko, A. Sampson-Johannes, K. Mondal, P. Ralph, and A. S. Baldwin. 1991. Characterization of an immediate-early gene induced in adherent monocytes that encodes IκB-like activity. Cell 65:1281.
14. Palombella, V. J., O. J. Rando, A. L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor prolein and the activation of NF-κB. Cell 78:773.
15. Li, C. H., R. Dai, and D. L. Longo 1995. Inactivation of NF-κB inhibitor IκBα: ubiquitin-dependent proteolysis and its degradation product. Biochem. Biophys. Res. Commun. 215:292.
16. Zandi, E., D. M. Rothwarf, M. Delhase, M. Hayakawa, and M. Karin. 1997. The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell 91:243.
17. Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. W. Li, D. B. Young, M. Barbosa, and M. Mann. 1997. IKK-1 and IKK-2: cytokine-Activated IκB kinases essential for NF-κB activation. Science 278:860.
18. Woronicz, J. D., X. Gao, Z. Cao, M. Rothe, and D. V. Goeddel. 1997. IκB Kinase-β: NF-κB activation and complex formation with IκB kinase-α and NIK. Science 278:866.
19. Stancovski, I., and D. Baltimore. 1997. NF-κB activation: the IκB kinase revealed? Cell 91:299.
20. Scherer, D. C., J. A. Brockman, Z. Chen, T. Maniatis, and D. W. Ballard. 1995. Signal-induced degradation of IκBα requires site-specific ubiquitination. Proc. Natl. Acad. Sci. USA 92:11259.
21. Finco, T. S., and A. S. Baldwin. 1995. Mechanistic aspects of NF-κB regulation: the emerging role of phosphorylation and proteolysis. Immunity 3:263.
22. Traenckner, E., H. Pahl, T. Henkel, K. 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.
23. Cai, Z., M. Körner, N. Tarantino, and S. Chouaib. 1997. IκBα overexpression in human breast carcinoma MCF7 cells inhibits nuclear factor-κB activation but not tumor necrosis factor-α-induced apoptosis. J. Biol. Chem. 272:96.
24. Ferreira, V., N. Tarantino, and M. Komer. 1998. Discrimination between Re1A and Re1B transcriptional regulation by a dominant negative mutant of IκBα. J. Biol. Chem. 273:592.
25. Köntgen, F., R. J. Grumont, A. Strasser, D. Metcalf, R. Li, D. Tarlinton, and S. Gerondakis. 1995. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9:1965.
26. Sha, W. C., H. C. Liou, E. I. Tuomanen, and D. Baltimore. 1995. Targeted disruption of the p50 subunit of NF-κB leads to multifocal defects in immune responses. Cell 80:321.
27. Franzoso, G., L. Carlson, L. Poljak, E. W. Shores, S. Epstein, A. Leonardi, A. Grinberg, T. Tran, T. Scharton-Kersten, M. Anver, et al. 1998. Mice deficient in nuclear factor (NF)-κB/p52 present with defects in humoral responses, germinal center reactions, and splenic microarchitecture. J. Exp. Med. 187:147.
28. Burkly, L., C. Hession, L. Ogata, C. Reilly, D. Marconi, D. Olson, R. Tizard, R. Cate, and D. Lo. 1995. Expression of Re1B is required for the development of Ihymic medulla and dendritic cells. Nature 373:531.
29. Weih, F., D. Carrasco, S. K. Durham, D. S. Barton, C. A. Rizzo, R. P. Ryseck, S. A. Lira, and R. Bravo. 1995. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of Re1B, a member of the NF-κB/Re1 family. Cell 80:331.
30. Beg, A. A., W. C. Sha, R. T. Bronson, S. Ghosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature 376:167.
31. Doi, T. S., T. Takahashi, O. Taguchi, T. Azumza, and Y. Obata. 1997. NF-κB Re1A-deficient lymphocytes: normal development of T cells and B cells, impaired production of IgA and IgG1 and reduced proliferative responses. J. Exp. Med. 185:953.
32. Tan, T. H., G. P. Huang, A. Sica, P. Ghosh, H. A. Young, D. L. Longo, and N. R. Rice. 1992. κB site-dependent activation of the interleukin-2 receptor-α-chain gene promoter by c-Re1. Mol. Cell. Biol. 12:4067.
33. Garoufalis, E., I. Kwan, R. Lin, A. Mustafa, N. Pepin, A. Roulston, J. Lacoste, and J. Hiscott. 1994. Viral induction of the human interferon promoter: modulation of transcription by NF-κB/Re1 proteins and interferon regulatory factors. J. Virol. 68:4707.
34. Boothby, M R., A. L. Mora, D. C. Scherer, J. A. Brockman, and D. W. Ballard. 1997. Perturbation of the T lymphocyte lineage in transgenic mice expressing a constitutive represser of nuclear factor (NF)-κB. J. Exp. Med 185:1897.
35. Esslinger, C. W., A. Wilson, B. Sordat, F. Beermann, and C. V. Jongeneel. 1997. Abnormal T lymphocyte development induced by targeted overexpression of IκBα. J. Immunol. 158:5075.
36. Allen, J. M., K. A. Forbush, and R. M. Perlmutter. 1992. Functional dissection of the lck proximal promoter. Mol. Cell. Biol. 12:2758.
37. Lewis, D. B., C. C. Yu, K. A. Forbush, J. Carpenter, T. A. Sato, A. Grossman, D. H. Liggitt, and R. M. Perlmutter. 1989. interleukin 4 expressed in situ selectively alters thymocyte development. J. Exp. Med. 173:89.
38. Transgenesis technics, principles and protocols. In Methods in Molecular Biology, Vol. 18. D. Murphy, and D. A. Carter, eds. Humana Press, Totowa, NJ, pp. 109-182.
39. Kruisberg, A. M. 1992. Isolation and fractionation of mononuclear cell populations. In Current Protocols in Immunology, Vol. 1. John Wiley & Sons, New York.
40. Jaffray, E, K. M. Wood, and R. T. Hay. 1995. Domain organization of IκBα and sites of interaction with NF-κB p65. Mol. Cell. Biol. 15:2166.
41. 2+-regulated kinase. Cytokine 3:257.
42. Leo, O., M. Foo, D. H. Sachs, L. E. Samelson, and J. A. Bluestone. 1987. Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proc. Natl. Acad. Sci. USA 91:123.
43. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156.
44. Coligan J. E., A. M. Kruisberg, D. H. Margulies, E. M. Shevach, and W. Strober. 1996. Current Protocols in Immunology, Vol. 1. John Wiley & Sons, New York.
45. Huang, H., J. Hu-Li, H. Chen, S. Z. Ben-Sasson, and W. E. Paul. 1997. IL-4 and IL-13 production in differentiated T helper type 2 cells is not IL-4 dependent. J. Immunol 159:3731.
46. Le Bail, O., R. Schmidt-Ullrich, and A. Israel. 1993. Promoter analysis of the gene encoding the IκBα/MAD3 inhibitor of NF-κB: positive regulation by members of the Re1/NF-κB family. EMBO J. 12:5043.
47. Ito, C. Y., A. G. Kazantzev, and A. S. Baldwin. 1994. Three NF-κB sites in the IκBa promoter are required for induction of gene expression. Nucleic Acids Res. 22:3787.
48. Cross, S. L., N. F. Halden, M. J. Lenardo, and W. J. Leonard. 1989. Functionally distinct NF-κB binding sites in the immunoglobulin κ and IL-2 receptor α chain genes. Science 244:466.
49. Verweij, C. L., M. Geerts, and L. A. Aarden. 1991. Activation of interleukin 2 gene transcription via the T-cell surface molecule CD28 is mediated through an NF-κB-like response element. J. Biol. Chem. 266:14179.
50. Lai, J. H., G. Horvath, J. Subleski, J. Bruder, P. Ghosh, and T. H. Tan. 1995. Re1 A is a potent transcriptional activator of the CD28 response element within the interleukin-2 promoter. Mol. Cell. Biol. 15:4260.
51. Sica, A., L. Dorman, V. Viggiano, M. Cippitelli, P. Gosh, N. Rice, and H. A. Young. 1997. Interaction of NF-κB and NFAT with the interferon-γ promoter. J. Biol. Chem. 272:30412.
52. Goldfeld, A. E., C. Doyle, and T. Maniatis. 1990. Human tumor necrosis factor α gene regulation by virus and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 87:9769.
53. Abbadie, C., N. Kabrun, J. F. Bouali, J. Smardova, D. Stehelin, B. Bandenbunder, and P. J. Enrietto. 1993. High levels of c-Re1 expression are associated with programmed cell death in the developing avian embryo and in bone marrow cells in vitro. Cell 75:899.
54. Beg, A. A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-α-induced cell death. Science 274:782.
55. Van Antwerp, D. J., S. J. Martin, T. Kafri, D. R. Green, and I. M. Verma. 1996. Suppression of TNF-α-induced apoptosis by NF-κB. Science 274:787.
56. Piqueras, B., B. Autran, P. Debré, and G. Gorochov. 1996. Detection of apoptosis at the single-cell level by direct incorporation of fluorescein-dUTP in DNA strand breaks. BioTechniques 20:634.
57. Attar, R. M., H. MacDonald-Bravo, C. Raventos-Suarez, S. K. Durham, and R. Bravo. 1998. Expression of constitutively active 1κBβ in T cells of transgenic mice: persistent NF-κB activity is required for T-cell immune responses. Mol. Cell. Biol. 18:477.
58. Veis, D. J., C.M. Sorenson, J. R. Shutter, and S. J. Korsmeyer. 1993. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75:229.
59. Ma, A., J. C. Pena, B. Chang, E. Margosian, L. Davidson, F. W. Alt, and C. B. Thompson. 1995. Bcl-x regulates the survival of double-positive thymocytes. Proc. Natl. Acad. Sci. USA 92:4763.
60. Motoyama, N., F. Wang, K. A. Roth, H. Sawa, K. I. Nakayama, I. Negishi, S. Senju, Q. Zhang, S. Fujii, and D. Y. Loh. 1995. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267:1506.
61. Van Parijs, L., A. Ibraghimov, and A. K. Abbas. 1996. The role of costimulation and Fas in T cells apoptosis and tolerance. Immunity 4:321.
62. Tucek-Szabo, C. L., S. Andjelic, E. Lacy, K. B. Elkon, and J. Nikolic-Zugic. 1996. Surface T cell Fas receptor/CD95 regulation, in vivo activation, and apoptosis: activation-induced death can occur without Fas receptor. J. Immunol. 156: 192.
63. Sytwu, H.-K., R. S. Liblau, and H. O. McDevitt. 1996. The roles of Fas/APO1 (CD95) and TNF in antigen-induced programmed cell receptor transgenic mice. Immunity 5:17.
64. Terada, N., J. J. Lucas, A. Szepesi, R. A. Franklin, J. Domenico, and E. W. Gelfand. 1993. Rapamycin blocks cell cycle progression of activated T cells prior to events characteristic of the middle to late G1 phase of the cycle. J. Cell. Physiol. 154:7.
65. Perkins, N. D., L. K. Felzien, J. C. Betts, K. Leung, D. H. Beach, and G. J. Nabel. 1997. Regulation of NF-κB by cyclin-dependent kinases associated with the p300 coactivator. Science 275:523.
66. Zhong, H., R. E. Voll, and S. Ghosh. 1998. Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1:661.
67. Bash, J., W. X. Zong, and C. Gelinas. 1997. C-Re1 arrests the proliferation of HeLa cells and affects critical regulators of the G1/S-phase transition. Mol. Cell. Biol. 17:6526.
68. Duckett, C. S., N. D. Perkins, K. Leung, A. B. Agranoff, and G. J. Nabel. 1995. Cytokine induction of nuclear factor κB in cycling and growth-arrested cells. J. Biol. Chem. 270:18836.
69. Casolaro, V., N. S. Georas, Z. Song, I. D. Zubkoff, S. A. Abdulkadir, D. Thanos, and S. J. Ono. 1995. Inhibition of NF-AT-dependent transcription by NF-κB: implications differential gene expression in T helper cell subsets. Immunology 92:11623.
70. Ishikawa, H., D. Carrasco, E. Claudio, R. P. Ryseck, and R. Bravo. 1997. Gastric hyperplasia and increased proliferative responses of lymphocytes in mice lacking the COOH-terminal ankyrin domain of NF-κB2. J. Exp. Med. 186:999.
71. Eskdale, J., D. Kube, H. Tesch, and G. Gallagher. 1997. Mapping of the human IL10 gene and further characterization of the 5′ flanking sequence. Immunogenetics 46:120.
72. Goldfeld A. E., J. L. Strominger, and C. Doyle. 1991. Human tumor necrosis factor a gene regulation in phorbol ester stimulated T and B cell lines. J. Exp. Med. 174:73.