RSK2 mediates NF-κB activity through the phosphorylation of IκBα in the TNF-R1 pathway

FASEB Journal

Volumn 24, Issue 9, 2010, Pages 3490-3499

  Peng, Cong ^a   Cho, Yong Yeon ^a   Zhu, Feng ^a   Xu, Yan Ming ^a   Wen, Weihong ^a   Ma, Wei Ya ^a   Bode, Ann M ^a   Dong, Zigang ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Apoptosis; Cell survival; Serine threonine kinases; Tumor promoter

Indexed keywords

I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RIBOSOMAL S6 KINASE 2; S6 KINASE; SERINE; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ANIMALS; CASPASE 3; CASPASE 8; CELL LINE; CELL LINE, TUMOR; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HELA CELLS; HUMANS; I-KAPPA B PROTEINS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICE; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77956624295     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-151290     Document Type: Article

References (47)

1. Kwon, B., Kim, B. S., Cho, H. R., Park, J. E., and Kwon, B. S. (2003) Involvement of tumor necrosis factor receptor superfamily(TNFRSF) members in the pathogenesis of inflammatory diseases. Exp. Mol. Med. 35, 8-16 (Pubitemid 36336923)
2. 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)
3. Chen, G., and Goeddel, D. V. (2002) TNF-R1 signaling: a beautiful pathway. Science 296, 1634-1635
4. Takeda, K., Stagg, J., Yagita, H., Okumura, K., and Smyth, M. J. (2007) Targeting death-inducing receptors in cancer therapy. Oncogene 26, 3745-3757 (Pubitemid 46842709)
5. Ashkenazi, A. (2002) Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat. Rev. Cancer 2, 420-430
6. Yang, P., McKay, B. S., Allen, J. B., and Jaffe, G. J. (2004) Effect of NF-kappa B inhibition on TNF-alpha-induced apoptosis in human RPE cells. Invest. Ophthalmol. Vis. Sci. 45, 2438-2446 (Pubitemid 38902620)
7. Geisler, F., Algul, H., Paxian, S., and Schmid, R. M. (2007) Genetic inactivation of RelA/p65 sensitizes adult mouse hepatocytes to TNF-induced apoptosis in vivo and in vitro. Gastroenterology 132, 2489-2503
8. Nakajima, A., Komazawa-Sakon, S., Takekawa, M., Sasazuki, T., Yeh, W. C., Yagita, H., Okumura, K., and Nakano, H. (2006) An antiapoptotic protein, c-FLIPL, directly binds to MKK7 and inhibits the JNK pathway. EMBO J. 25, 5549-5559 (Pubitemid 44847195)
9. Micheau, O., Lens, S., Gaide, O., Alevizopoulos, K., and Tschopp, J. (2001) NF-kappaB signals induce the expression of c-FLIP. Mol. Cell. Biol. 21, 5299-5305 (Pubitemid 32702435)
10. Li, X., Yang, Y., and Ashwell, J. D. (2002) TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2. Nature 416, 345-347
11. Naismith, J. H., and Sprang, S. R. (1998) Modularity in the TNF-receptor family. Trends Biochem. Sci. 23, 74-79
12. Ashkenazi, A., and Dixit, V. M. (1998) Death receptors: signaling and modulation. Science 281, 1305-1308
13. Ghosh, S., and Karin, M. (2002) Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl.), S81-S96
14. Hatada, E. N., Nieters, A., Wulczyn, F. G., Naumann, M., Meyer, R., Nucifora, G., McKeithan, T. W., and Scheidereit, C. (1992) The ankyrin repeat domains of the NF-kappa B precursor p105 and the protooncogene bcl-3 act as specific inhibitors of NF-kappa B DNA binding. Proc. Natl. Acad. Sci. U. S. A. 89, 2489-2493
15. Johnson, C., Van Antwerp, D., and Hope, T. J. (1999) An N-terminal nuclear export signal is required for the nucleocytoplasmic shuttling of IkappaBalpha. EMBO J. 18, 6682-6693
16. Micheau, O., and Tschopp, J. (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181-190 (Pubitemid 36936912)
17. Karin, M., and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18, 621-663 (Pubitemid 30365393)
18. Swanson, K. D., Taylor, L. K., Haung, L., Burlingame, A. L., and Landreth, G. E. (1999) Transcription factor phosphorylation by pp90(rsk2). Identification of Fos kinase and NGFI-B kinase I as pp90(rsk2). J. Biol. Chem. 274, 3385-3395
19. Sassone-Corsi, P., Mizzen, C. A., Cheung, P., Crosio, C., Monaco, L., Jacquot, S., Hanauer, A., and Allis, C. D. (1999) Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. Science 285, 886-891
20. Mahadevan, L. C., Clayton, A. L., Hazzalin, C. A., and Thomson, S. (2004) Phosphorylation and acetylation of histone H3 at inducible genes: two controversies revisited. Novartis Found. Symp. 259, 102-111; discussion 111-104, 163-109
21. Anjum, R., Roux, P. P., Ballif, B. A., Gygi, S. P., and Blenis, J. (2005) The tumor suppressor DAP kinase is a target of RSK-mediated survival signaling. Curr. Biol. 15, 1762-1767 (Pubitemid 41415634)
22. Bonni, A., Brunet, A., West, A. E., Datta, S. R., Takasu, M. A., and Greenberg, M. E. (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286, 1358-1362
23. Palmer, A., Gavin, A. C., and Nebreda, A. R. (1998) A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34 (cdc2) inhibitory kinase Myt1. EMBO J. 17, 5037-5047
24. Xing, J., Ginty, D. D., and Greenberg, M. E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963
25. Yang, X., Matsuda, K., Bialek, P., Jacquot, S., Masuoka, H. C., Schinke, T., Li, L., Brancorsini, S., Sassone-Corsi, P., Townes, T. M., Hanauer, A., and Karsenty, G. (2004) ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry Syndrome. Cell 117, 387-398 (Pubitemid 38534544)
26. Cho, Y. Y., Yao, K., Bode, A. M., Bergen, H. R., 3rd, Madden, B. J., Oh, S. M., Ermakova, S., Kang, B. S., Choi, H. S., Shim, J. H., and Dong, Z. (2007) RSK2 mediates muscle cell differentiation through regulation of NFAT3. J. Biol. Chem. 282, 8380-8392
27. Cho, Y. Y., He, Z., Zhang, Y., Choi, H. S., Zhu, F., Choi, B. Y., Kang, B. S., Ma, W. Y., Bode, A. M., and Dong, Z. (2005) The p53 protein is a novel substrate of ribosomal S6 kinase 2 and a critical intermediary for ribosomal S6 kinase 2 and histone H3 interaction. Cancer Res. 65, 3596-3603 (Pubitemid 40616335)
28. Willard, F. S., and Crouch, M. F. (2001) MEK, ERK, and p90RSK are present on mitotic tubulin in Swiss 3T3 cells: a role for the MAP kinase pathway in regulating mitotic exit. Cell. Signal. 13, 653-664
29. Cho, Y. Y., Yao, K., Kim, H. G., Kang, B. S., Zheng, D., Bode, A. M., and Dong, Z. (2007) Ribosomal S6 kinase 2 is a key regulator in tumor promoter induced cell transformation. Cancer Res. 67, 8104-8112 (Pubitemid 47395145)
30. Eisinger-Mathason, T. S., Andrade, J., Groehler, A. L., Clark, D. E., Muratore-Schroeder, T. L., Pasic, L., Smith, J. A., Shabanowitz, J., Hunt, D. F., Macara, I. G., and Lannigan, D. A. (2008) Codependent functions of RSK2 and the apoptosis-promoting factor TIA-1 in stress granule assembly and cell survival. Mol. Cell 31, 722-736
31. Kang, S., Dong, S., Gu, T. L., Guo, A., Cohen, M. S., Lonial, S., Khoury, H. J., Fabbro, D., Gilliland, D. G., Bergsagel, P. L., Taunton, J., Polakiewicz, R. D., and Chen, J. (2007) FGFR3 activates RSK2 to mediate hematopoietic transformation through tyrosine phosphorylation of RSK2 and activation of the MEK/ERK pathway. Cancer Cell 12, 201-214 (Pubitemid 47333416)
32. Sethi, G., Ahn, K. S., Chaturvedi, M. M., and Aggarwal, B. B. (2007) Epidermal growth factor (EGF) activates nuclear factor-kappaB through IkappaBalpha kinase-independent but EGF receptor-kinase dependent tyrosine 42 phosphorylation of IkappaBalpha. Oncogene 26, 7324-7332
33. Bjorbaek, C., Zhao, Y., and Moller, D. E. (1995) Divergent functional roles for p90rsk kinase domains. J. Biol. Chem. 270, 18848-18852
34. Fisher, T. L., and Blenis, J. (1996) Evidence for two catalytically active kinase domains in pp90rsk. Mol. Cell. Biol. 16, 1212-1219 (Pubitemid 26064460)
35. Merienne, K., Jacquot, S., Zeniou, M., Pannetier, S., Sassone-Corsi, P., and Hanauer, A. (2000) Activation of RSK by UV-light: phosphorylation dynamics and involvement of the MAPK pathway. Oncogene 19, 4221-4229
36. Smith, J. A., Poteet-Smith, C. E., Malarkey, K., and Sturgill, T. W. (1999) Identification of an extracellular signal-regulated kinase (ERK) docking site in ribosomal S6 kinase, a sequence critical for activation by ERK in vivo. J. Biol. Chem. 274, 2893-2898
37. Dalby, K. N., Morrice, N., Caudwell, F. B., Avruch, J., and Cohen, P. (1998) Identification of regulatory phosphorylation sites in mitogen-activated protein kinase (MAPK)-activated protein kinase-1a/p90rsk that are inducible by MAPK. J. Biol. Chem. 273, 1496-1505 (Pubitemid 28133672)
38. Vik, T. A., and Ryder, J. W. (1997) Identification of serine 380 as the major site of autophosphorylation of Xenopus pp90rsk. Biochem. Biophys. Res. Commun. 235, 398-402
39. Frodin, M., Antal, T. L., Dummler, B. A., Jensen, C. J., Deak, M., Gammeltoft, S., and Biondi, R. M. (2002) A phosphoserine/threonine-binding pocket in AGC kinases and PDK1 mediates activation by hydrophobic motif phosphorylation. EMBO J. 21, 5396-5407
40. Frodin, M., Jensen, C. J., Merienne, K., and Gammeltoft, S. (2000) A phosphoserine-regulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J. 19, 2924-2934
41. Jensen, C. J., Buch, M. B., Krag, T. O., Hemmings, B. A., Gammeltoft, S., and Frodin, M. (1999) 90-kDa ribosomal S6 kinase is phosphorylated and activated by 3-phosphoinositide-dependent protein kinase-1. J. Biol. Chem. 274, 27168-27176
42. Chen, Z., Hagler, J., Palombella, V. J., Melandri, F., Scherer, D., Ballard, D., and Maniatis, T. (1995) Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9, 1586-1597
43. Brown, K., Gerstberger, S., Carlson, L., Franzoso, G., and Siebenlist, U. (1995) Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267, 1485-1488
44. Chen, N., Nomura, M., She, Q. B., Ma, W. Y., Bode, A. M., Wang, L., Flavell, R. A., and Dong, Z. (2001) Suppression of skin tumorigenesis in c-Jun NH(2)-terminal kinase-2-deficient mice. Cancer Res. 61, 3908-3912
45. Choi, H. S., Bode, A. M., Shim, J. H., Lee, S. Y., and Dong, Z. (2009) JNK1 phosphorylates Myt1 to prevent UVA-induced skin cancer. Mol. Biol. Cell 29, 2168-2180
46. She, Q. B., Chen, N., Bode, A. M., Flavell, R. A., and Dong, Z. (2002) Deficiency of c-Jun-NH(2)-terminal kinase-1 in mice enhances skin tumor development by 12-O-tetradecanoylphorbol-13-acetate. Cancer Res. 62, 1343-1348
47. Bignone, P. A., Lee, K. Y., Liu, Y., Emilion, G., Finch, J., Soosay, A. E., Charnock, F. M., Beck, S., Dunham, I., Mungall, A. J., and Ganesan, T. S. (2007) RPS6KA2, a putative tumour suppressor gene at 6q27 in sporadic epithelial ovarian cancer. Oncogene 26, 683-700