Beyond IκBs: Alternative regulation of NF-κB activity

FASEB Journal

Volumn 21, Issue 11, 2007, Pages 2642-2654

  Neumann, Manfred ^a   Naumann, Michael ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Dimer exchange; GR NF B cross talk; Nucleolar sequestration; RelA acetylation; RelA phosphorylation

Indexed keywords

CASEIN KINASE II; GLUCOCORTICOID RECEPTOR; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; PROTEIN P50; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB; TRANSCRIPTION FACTOR SP1; UBIQUITIN; ZINC FINGER PROTEIN; DNA BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS INCLUSION BODY; COMPLEX FORMATION; DIMERIZATION; GENE CONTROL; LEUKEMIA CELL LINE; NONHUMAN; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ANIMAL; DRUG ANTAGONISM; HUMAN; METABOLISM; PHOSPHORYLATION;

ANIMALS; DNA-BINDING PROTEINS; HUMANS; I-KAPPA B PROTEINS; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; UBIQUITINS;

EID: 34548487143     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7615rev     Document Type: Review

References (97)

1. Hayden, M. S., and Ghosh, S. (2004) Signaling to NF-κB. Genes Dev. 18, 2195-2224
2. Gilmore, T. D. (2006) Introduction to NF-κB: players, pathways, perspectives. Oncogene 25, 6680-6684
3. Strober, W., Murray, P. J., Kitani, A., and Watanabe, T. (2006) Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6, 9-20
4. Janssens, S., and Tschopp, J. (2006) Signals from within: the DNA-damage-induced NF-κB response. Cell Death Differ. 13, 773-784 (review)
5. Wu, C.-J., Conze, D. B., Li, T., Srinivasula, S. M., and Ashwell, J. D. (2006) Sensing of Lys 63-linked polyubiquitinylation by NEMO is a key event in NF-κB activation. Nat. Cell Biol. 8, 398-406
6. Ea, C.-K., Deng, L., Xia, Z.-P., Pineda, G., and Chen, Z. J. (2006) Activation of IKK by TNFα requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22, 245-257
7. Chen, F., Bhatia, D., and Castranova, V. (2006) Finding NEMO by K63-linked polyubiquitin chain. Cell Death Differ. 13, 1835-1838
8. Kato, T., Jr., Delhase, M., Hoffmann, A., and Karin, M. (2003) CK2 is a C-terminal IκB kinase responsible for NF-κB activation during UV response. Mol. Cell 12, 829-839
9. Wuerzberger-Davis, S. M., Nakamura, Y., Seufzer, B. J., and Miyamoto, S. (2007) NF-κB activation by combinations of NEMO sumoylation and ATM activation stresses in the absence of DNA damage. Oncogene 26, 641-651
10. Huang, T. T., Wuerzberger-Davis, S. M., Wu, Z.-H., and Miyamoto, S. (2003) Sequential modification of NEMO/IKKγ by SUMO-1 and ubiquitin mediates NF-κB activation by genotoxic stress. Cell 115, 565-576
11. Janssens, S., Tinel, A., Lippens, S., and Tschopp, J. (2005) PIDD mediates NF-κB activation in response to DNA damage. Cell 123, 1-14
12. Mabb, A. M., Wuerzberger-Davis, S. M., and Miyamoto, S. (2006) PIASy mediates NEMO sumoylation and NF-κB activation in response to genotoxic stress. Nat. Cell Biol. 8, 986-993
13. Wu, Z.-H., Shi, Y., Tibbetts, R. S., and Miyamoto, S. (2006) Molecular linkage between the kinase ATM and NF-κB signaling in response to genotoxic stimuli. Science 311, 1141-1146
14. Karin, M., and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitinylation: the control of NF-κB activity. Annu. Rev. Immunol. 18, 621-663
15. Gao, M., and Karin, M. (2005) Regulating the regulators: control of protein ubiquitinylation and ubiquitin-like modifications by extracellular stimuli. Mol. Cell 19, 581-593
16. Heynick, K., and Beyaert, R. (2005) A20 inhibits NF-κB activation by dual ubiquitin-editing functions. Trends Biochem. Sci. 30, 1-4
17. Lee, E. G., Boone, D. L., Chai, S., Libby, S. L., Chien, M., Lodolce, J. P., and Ma, A. (2000) Failure to regulate TNF-induced NF-κB and cell death responses in A20-deficient mice. Science 289, 2350-2354
18. Wertz, I. E., O'Rourke, K. M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., Wu, P., Wiesmann, C., Baker, R., Boone, D. L., Ma, A., et al. (2004) De-ubiquitinylation and ubiquitin ligase domains of A20 downregulate NF-κB signalling. Nature 430, 694-699
19. Mauro, C., Pacifico, F., Lavorgna, A., Mellone, S., Iannetti, A., Acquaviva, R., Formisano, S., Vito, P., and Leonardi, A. (2006) ABIN-1 binds to NEMO/IKKγ and co-operates with A20 in inhibiting NF-κB. J. Biol. Chem. 281, 18482-18488
20. Viatour, P., Merville, M.-P., Bours, V., and Chariot, A. (2005) Phosphorylation of NF-κB and IκB proteins: implications in cancer and inflammation. Trends Biochem. Sci. 30, 43-52
21. Perkins, N. D. (2006) Post-translational modifications regulating the activity and function of the NF-κB pathway. Oncogene 25, 6717-6730
22. Mellits, K. H., Hay, R. T., and Goodbourn, S. (1993) Proteolytic degradation of MAD3 (IκBα) and enhanced processing of the NF-κB precursor p105 are obligatory steps in the activation of NF-κB. Nucleic Acids Res. 21, 5059-5066
23. Naumann, M., and Scheidereit, C. (1994) Activation of NF-κB in vivo is regulated by multiple phosphorylations. EMBO J. 13, 4597-4607
24. Sakurai, H., Chiba, H., Miyoshi, H., Sugita, T., and Toriumi, W. (1999) IκB kinases phosphorylate NF-κB p65 subunit on serine 536 in the transactivation domain. J. Biol. Chem. 274, 30353-30356
25. O'Mahony, A. M., Montano, M., vanBeneden, K., Chen, L. F., and Greene, W. C. (2004) Human T-cell lymphotropic virus type 1 tax induction of biologically active NF-κB requires IκB kinase-1-mediated phosphorylation of RelA/p65. J. Biol. Chem. 279, 18137-18145
26. Jiang, X., Takahashi, N., Matsui, N., Tetsuka, T., and Okamoto, T. (2003) The NF-κB activation in lymphotoxin β receptor signaling depends on the phosphorylation of p65 at serine 536. J. Biol. Chem. 278, 919-926
27. Buss, H., Dorrie, A., Schmitz, M. L., Hoffmann, E., Resch, K., and Kracht, M. (2004) Constitutive and interleukin-1-inducible phosphorylation of p65 NF-κB at serine 536 is mediated by multiple protein kinases including IκB kinases IKKα, IKKβ, IKKε, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J. Biol. Chem. 279, 55633-55643
28. Fujita, F., Taniguchi, Y., Kato, T., Narita, Y., Furuya, A., Ogawa, T., Sakurai, H., Joh, T., Itoh, M., Delhase, M., Karin, M., and Nakanishi, M. (2003) Identification of NAP1, a regulatory subunit of IκB kinase-related kinases that potentiates NF-κB signaling. Mol. Cell Biol. 23, 7780-7793
29. Adli, M., and Baldwin, A. S. (2006) IKK-i/IKKε controls constitutive, cancer cell-associated NF-κB activity via regulation of Ser-536 p65/RelA phosphorylation. J. Biol. Chem. 281, 26976-26984
30. Bohuslav, J., Chen, L. F., Kwon, H., Mu, Y., and Greene, W. C. (2004) p53 induces NF-κB activation by an IκB kinase-independent mechanism involving phosphorylation of p65 by ribosomal S6 kinase 1. J. Biol. Chem. 279, 26115-26125
31. Sasaki, C. Y., Barberi, T. J., Ghosh, P., and Longo, D. L. (2005) Phosphorylation of RelA/p65 on serine 536 defines an IκBα- independent NF-κB pathway. J. Biol. Chem. 280, 34538-34547
32. Qin, C., Nguyen, T., Stewart, J., Samudio, I., Burghardt, R., and Safe, S. (2002) Estrogen up-regulation of p53 gene expression in MCF-7 breast cancer cells is mediated by calmodulin kinase IV-dependent activation of a NF-κB/CCAAT-binding transcription factor-1 complex. Mol. Endocrinol. 16, 1793-1809
33. Bae, J. S., Jang, M. K., Hong, S., An, W. G., Choi, Y. H., Kim, H. D., and Cheong, J. (2003) Phosphorylation of NF-κB by calmodulin-dependent kinase IV activates anti-apoptotic gene expression. Biochem. Biophys. Res. Commun. 305, 1094-1098
34. Bird, T. A., Schooley, K., Dower, S. K., Hagen, H., and Virca, G. D. (1997) Activation of nuclear transcription factor NF-κB by interleukin-1 is accompanied by casein kinase II-mediated phosphorylation of the p65 subunit. J. Biol. Chem. 272, 32606-32612
35. Wang, D., Westerheide, S. D., Hanson, J. L., and Baldwin, A. S., Jr. (2000) Tumor necrosis factor alpha-induced phosphorylation of RelA/p65 on Ser529 is controlled by casein kinase II. J. Biol. Chem. 275, 32592-32596
36. Schwabe, R. F., and Sakurai, H. (2006) IKKβ phosphorylates p65 at S468 in transactivation domain 2. FASEB J. 19, 1758-1760
37. Mattioli, I., Geng, H., Sebald, A., Hodel, M., Bucher, C., Kracht, M., and Schmitz, M. L. (2006) Inducible phosphorylation of NF-κB p65 at serine 468 by T cell costimulation is mediated by IKKε. J. Biol. Chem. 281, 6175-6183
38. Buss, H., Dörrie, A., Schmitz, M. L., Frank, R., Livingstone, M., Resch, K., and Kracht, M. (2004) Phosphorylation of serine 468 by GSK-3β negatively regulates basal p65 NF-κB activity. J. Biol. Chem. 279, 49571-49574
39. Bournat, J. C., Brown, A. M., and Soler, A. P. (2000) Wnt-1 dependent activation of the survival factor NF-κB in PC12 cells. J. Neurosci. Res. 61, 21-32
40. Sanchez, J. F., Sniderhan, L. F., Williamson, L. F., Fan, S., Chakraborty-Sett, S., and Maggirwar, S. B. (2003) Glycogen synthase kinase 3β-mediated apoptosis of primary cortical astrocytes involves inhibition of NF-κB signaling. Mol. Cell. Biol. 23, 4649-4662
41. Hoeflich, K. P., Luo, J., Rubie, E. A., Tsao, M. S., Jin, O., and Woodgett, J. R. (2000) Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 206, 86-90
42. Duran, A., Diaz-Meco, M. T., and Moscat, J. (2003) Essential role of RelA Ser311 phosphorylation by zetaPKC in NF-κB transcriptional activation. EMBO J. 22, 3910-3918
43. Zhong, H., SuYang, H., Erdjument-Bromage, H., Tempst, P., and Ghosh, S. (1997) The transcriptional activity of NF-κB is regulated by the IκB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89, 413-424
44. Vermeulen, L., De Wilde, G., van Damme, P., van den Berghe, W., and Haegeman, G. (2003) Transcriptional activation of the NF-κB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 22, 1313-1324
45. Zhong, H., May, M. J., Jimi, E., and Ghosh, S. (2002) The phosphorylation status of nuclear NF-κB determines its association with CBP/p300 or HDAC-1. Mol. Cell 9, 625-636
46. Jacque, E., Tchenio, T., Piton, G., Romeo, P. H., and Baud, V. (2005) RelA repression of RelB activity induces selective gene activation downstream of TNF receptors. Proc. Natl. Acad. Sci. U. S. A. 102, 14635-14640
47. Yeh, P. Y., Yeh, K. H., Chuang, S. E., Song, Y. C., and Cheng, A. L. (2004) Suppression of MEK/ERK signaling pathway enhances cisplatin-induced NF-κB activation by protein phosphatase 4-mediated NF-κB p65 Thr dephosphorylation. J. Biol. Chem. 279, 26143-26148
48. Rocha, S., Garrett, M. D., Campbell, K. J., Schumm, K., and Perkins, N. D. (2005) Regulation of NF-κB and p53 through activation of ATR and Chk1 by the ARF tumour suppressor. EMBO J. 24, 1157-1169
49. Campbell, K. J., Witty, J. M., Rocha, S., and Perkins, N. D. (2006) Cisplatin mimics ARF tumor suppressor regulation of RelA (p65) NF-κB transactivation. Cancer Res. 66, 929-935
50. Ryo, A., Suizu, F., Yoshida, Y., Perrem, K., Liou, Y. C., Wulf, G., Rottapel, R., Yamaoka, S., and Lu, K. P. (2003) Regulation of NF-κB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol. Cell 12, 1413-1426
51. Maine, G. N., Mao, X., Komarck, C. M., and Burstein, E. (2007) COMMD1 promotes the ubiquitination of NF-κB subunits through a cullin-containing ubiquitin ligase. EMBO J. 26, 436-447
52. Lawrence, T., Bebien, M., Liu, G. Y., Nizet, V., and Karin, M. (2005) IKKα limits macrophage NF-κB activation and contributes to the resolution of inflammation. Nature 434, 1138-1143
53. Nelson, D. E., Ihekwaba, A. E., Elliot, M., Johnson, J. R., Gibney, C. A., Foreman, B. E., Nelson, G., See, V., Horton, C. A., Spiller, D. G., et al. (2004) Oscillations in NF-κB signaling control the dynamics of gene expression. Science 306, 704-708
54. Liu, Y., Denlinger, C. E., Rundall, B. K., Smith, P. W., and Jones, D. R. (2006) Suberoylanilide hydroxamic acid induces Aktmediated phosphorylation of p300, which promotes acetylation and transcriptional activation of RelA/p65. J. Biol. Chem. 281, 31359-31368
55. Hoberg, J. E., Popko, A. E., Ramsey, C. S., and Mayo, M. W. (2006) IKKα-mediated derepression of SMRT potentiates acetylation of RelA/p65 by p300. Mol. Cell Biol. 26, 457-471
56. Chen, L. F., Mu, Y., and Greene, W. C. (2002) Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-κB. EMBO J. 21, 6539-6548
57. Yeung, F., Hoberg, J. E., Ramsey, C. S., Keller, M. D., Jones, D. R., Frye, R. A., and Mayo, M. W. (2004) Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 23, 2369-2380
58. Kiernan, R., Bres, V., Nig, R. W., Coudart, M. P., El Messaoudi, S., Sardet, C., Jin, D. Y., Emiliani, S., and Benkirane, M. (2003) Post-activation turn-off of NF-κB-dependent transcription is regulated by acetylation of p65. J. Biol. Chem. 278, 2758-2766
59. Chen, L. F., Williams, S. A., Mu, Y., Nakano, H., Duerr, J. M., Buckbinder, L., and Greene, W. C. (2005) NF-κB RelA phosphorylation regulates RelA acetylation. Mol. Cell. Biol. 25, 7966-7975
60. Huang, D. B., Vu, D., and Gosh, G. (2005) NF-κB RelB forms an intertwined homodimer. Structure 13, 1365-1373
61. Marienfeld, R., Berberich-Siebelt, F., Berberich, I., Denk, A., Serfling, E., and Neumann, M. (2001) Signal-specific and phosphorylation-dependent RelB degradation: a potential mechanism of NF-κB control. Oncogene 20, 8142-8147
62. Maier, H. J., Marienfeld, R., Wirth, T., and Baumann, B. (2003) Critical role of RelB serine 368 for dimerization and p100 stabilization. J. Biol. Chem. 278, 39242-39250
63. Druker, B. J., Neumann, M., Okuda, K., Franza, B. R., Jr., and Griffin, J. D. (1994) rel Is rapidly tyrosine-phosphorylated following granulocyte-colony stimulating factor treatment of human neutrophils. J. Biol. Chem. 269, 5387-5390
64. Fognani, C., Rondi, R., Romano, A., and Blasi, F. (2000) cRel-TD kinase: a serine/threonine kinase binding in vivo and in vitro c-Rel and phosphorylating its transactivation domain. Oncogene 19, 2224-2232
65. Martin, A. G., and Fresno, M. (2000) Tumor necrosis factoralpha activation of NF-κB requires the phosphorylation of Ser-471 in the transactivation domain of c-Rel. J. Biol. Chem. 275, 24383-24391
66. Yu, S. H., Chiang, W. C., Shih, H. M., and Wu, K. J. (2004) Stimulation of c-Rel transcriptional activity by PKA catalytic subunit beta. J. Mol. Med. 82, 621-628
67. Martin, A. G., San-Antonio, B., and Fresno, M. (2001) Regulation of NF-κB transactivation. Implication of phosphatidylinositol 3-kinase and PKCζ in c-Rel activation by TNFα. J. Biol. Chem. 276, 15840-15849
68. Starczynowski, D. T., Reynolds, J. G., and Gilmore, T. D. (2005) Mutations of TNFα-responsive serine residues within the Cterminal transactivation domain of human transcription factor REL enhance its in vitro transforming ability. Oncogene 24, 7355-7368
69. Starczynowski, D. T., Trautmann, H., Pott, C., Harder, L., Arnold, N., Africa, J. A., Leeman, J. R., Siebert, R., and Gilmore, T. D. (2006) Mutation of an IKK phosphorylation site within the transactivation domain of REL in two patients with B-cell lymphoma enhances REL's in vitro transforming activity. Oncogene In press
70. Harris, J., Oliere, S., Sharma, S., Sun, Q., Lin, R., Hiscott, J., and Grandvaux, N. (2006) Nuclear accumulation of c-Rel following C-terminal phosphorylation by TBK1/IKKε. J. Immunol. 177, 2527-2535
71. Sanchez-Valdepenas, C., Martin, A. G., Ramakrishnan, P., Wallach, D., and Fresno, M. (2006) NF-κB-inducing kinase is involved in the activation of the CD28 responsive element through phosphorylation of c-Rel and regulation of its transactivating activity. J. Immunol. 176, 4666-4674
72. Guan, H., Hou, S., and Ricciardi, R. P. (2005) DNA binding of repressor NF-κB p50/p50 depends on phosphorylation of Ser337 by the protein kinase A catalytic subunit. J. Biol. Chem. 280, 9957-9962
73. Zwergal, A., Quirling, M., Saugel, B., Huth, K. C., Sydlik, C., Poli, V., Neumeier, D., Ziegler-Heitbrock, H. W., and Brand, K. (2006) C/EBP beta blocks p65 phosphorylation and thereby NF-κB-mediated transcription in TNF-tolerant cells. J. Immunol. 177, 665-672
74. Gao, F., Cheng, J., Shi, T., and Yeh, E. T. (2006) Neddylation of a breast cancer-associated protein recruits a class III histone deacetylase that represses NF-κB-dependent transcription. Nat. Cell Biol. 8, 1171-1178
75. Adcock, I. M., Ito, K., and Barnes, P. J. (2004) Glucocorticoids: effects on gene transcription. Proc. Am. Thorac. Soc. 1, 247-254
76. De Bosscher, K., Vanden Berghe, W., and Haegeman, G. (2006) Cross-talk between nuclear receptors and NF-κB. Oncogene 25, 6868-6886
77. De Bosscher, K., Vanden Berghe, W., and Haegeman, G. (2003) The interplay between the glucocorticoid receptor and NF-κB or AP-1: molecular mechanisms for gene repression. Endocr. Rev. 24, 488-522
78. Martens, C., Bilodeau, S., Maira, M., Gauthier, Y., and Drouin, J. (2005) Protein-protein interactions and transcriptional antagonism between the subfamily of NGFI-B/Nur77 orphan nuclear receptors and glucocorticoid receptor. Mol. Endocrinol. 19, 885-897
79. Liden, J., Rafter, I., Truss, M., Gustafsson, J. A., and Okret, S. (2000) Glucocorticoid effects on NF-κB binding in the transcription of the ICAM-1 gene. Biochem. Biophys. Res. Commun. 273, 1008-1014
80. Nissen, R. M., and Yamamoto, K. R. (2000) The glucocorticoid receptor inhibits NF-κB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 14, 2314-2329
81. Park, K. J., Krishnan, V., O'Malley, B. W., Yamamoto, Y., and Gaynor, R. B. (2005) Formation of an IKKα-dependent transcription complex is required for estrogen receptor-mediated gene activation. Mol. Cell 18, 71-82
82. Park, G. Y., Wang, X., Hu, N., Pedchenko, T. V., Blackwell, T. S., and Christman, J. W. (2006) NIK is involved in nucleosomal regulation by enhancing histone H3 phosphorylation by IKKα. J. Biol. Chem. 281, 18684-18690
83. Ito, K., Barnes, P. J., and Adcock, I. M. (2000) Glucocorticoid receptor recruitment of HDAC 2 inhibits interleukin-1β-induced histone H4 acetylation on lysines 8 and 12. Mol. Cell. Biol. 20, 6891-6903
84. Garside, H., Stevens, A., Farrow, S., Normand, C., Houle, B., Berry, A., Maschera, B., and Ray, D. (2004) Glucocorticoid ligands specify different interactions with NF-κB by allosteric effects on the glucocorticoid receptor DNA binding domain. J. Biol. Chem. 279, 50050-50059
85. Luecke, H. F., and Yamamoto, K. R. (2005) The glucocorticoid receptor blocks P-TEFb recruitment by NF-κB to effect promoter-specific transcriptional repression. Genes Dev. 19, 1116-1127
86. Rubbi, C. P., and Milner, J. (2000) Non-activated p53 colocalizes with sites of transcription within both the nucleoplasm and the nucleolus. Oncogene 19, 85-96
87. Weber, J. D., Kuo, M. L., Bothner, B., DiGiammarino, E. L., Kriwacki, R. W., Russel, M. F., and Sherr, C. J. (2000) Cooperative signals governing ARF-Mdm2 interaction and nucleolar localization of the complex. Mol. Cell. Biol. 20, 2517-2528
88. Datta, A., Nag, A., Pan, W., Hay, N., Gartel, A. L., Colamonici, O., Mori, Y., and Raychaudhuri, P. (2004) Myc-ARF interaction inhibits the functions of Myc. J. Biol. Chem. 35, 36698-36707
89. Birbach, A., Bailey, S. T., Ghosh, S., and Schmid, J. A. (2004) Cytosolic, nuclear and nucleolar localization signals determine subcellular distribution and activity of the NF-κB inducing kinase NIK. J. Cell Sci. 117, 3615-3624
90. Niedick, I., Froese, N., Oumard, A., Müller, P. P., Nourbakhsh, M., Hauser, H., and Koster, M. (2004) Nucleolar localization and mobility analysis of the NF-κB repressing factor NRF. J. Cell Sci. 117, 3447-3458
91. Sweet, T., Khalili, K., Sawaya, B. E., and Amini, S. (2003) Identification of a novel protein from glia cells based on its ability to interact with NF-κB subunits. J. Cell Biochem. 90, 884-891
92. Dhar, S. K., Lynn, B. C., Daosukho, C., and St. Clair, D. K. (2004) Identification of nucleophosmin as an NF-κB co-activator for the induction of the human SOD2 gene. J. Biol. Chem. 279, 28209-28219
93. Stark, L., and Dunlop, M. G. (2005) Nucleolar sequestration of RelA (p65) regulates NF-κB-driven transcription and apoptosis. Mol. Cell. Biol. 25, 5985-6004
94. Saccani, S., Pantano, S., and Natoli, G. (2003) Modulation of NF-κB activity by exchange of dimers. Mol. Cell 11, 1563-1574
95. Saccani, S., Marazzi, I., Beg, A. A., and Natoli, G. (2004) Degradation of promoter-bound p65/RelA is essential for the prompt termination of the nuclear factor kappaB response. J. Exp. Med. 200, 107-113
96. Taganov, K. D., Boldin, M. P., Chang, K.-J., and Baltimore, D. (2006) NF-B-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 103, 12481-12486
97. Rayet, B., Fan, Y., and Gelinas, C. (2003) Mutations in the v-Rel transactivation domain indicate altered phosphorylation and identify a subset of NF-κB-regulated cell death inhibitors important for v-Rel transforming activity. Mol. Cell. Biol. 23, 1520-1533