Phosphorylation of NF-κB proteins by cyclic GMP-dependent kinase: A noncanonical pathway to NF-κB activation

European Journal of Biochemistry

Volumn 270, Issue 10, 2003, Pages 2174-2185

  He, Bin ^a   Weber, Georg F ^a,b  

^a TUFTS MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Protein kinases; Signal transduction; Superantigens; Transcription factors

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC GMP DEPENDENT PROTEIN KINASE; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P50; PROTEIN P52; SYNAPTOTAGMIN; COMPLEMENTARY DNA; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR RELA;

APOPTOSIS; ARTICLE; BINDING SITE; CELL DEATH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA BINDING; DOSE RESPONSE; ENHANCER REGION; ENZYME ACTIVATION; ENZYME SUBSTRATE COMPLEX; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STRESS; TRANSACTIVATION; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; CELL NUCLEUS; CHEMISTRY; ENZYME SPECIFICITY; GENETIC TRANSFECTION; KIDNEY; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MOUSE; PHOSPHORYLATION; REPORTER GENE; T LYMPHOCYTE; TIME; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; CLONING, MOLECULAR; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DNA, COMPLEMENTARY; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENES, REPORTER; HUMANS; KIDNEY; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; PHOSPHORYLATION; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; T-LYMPHOCYTES; TIME FACTORS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR RELA; TRANSFECTION;

EID: 0037517100     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03574.x     Document Type: Article

References (42)

1. Sen, R. & Baltimore, D. (1986) Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46, 705-716.
2. Sen, R. & Baltimore, D. (1986) Inducibility of κ immunoglobulin enhancer-binding protein NF-κB by a posttranslational mechanism. Cell 47, 921-928.
3. Weber, G.F., Abromson-Leeman, S. & Cantor, H. (1995) A signalling pathway coupled to T cell receptor ligation by MMTV superantigen leading to transient activation and programmed cell death. Immunity 2, 363-372.
4. Kim, D., Xu, M., Nie, L., Peng, X.C., Jimi, E., Voll, R.E., Nguyen, T., Ghosh, S. & Sun, X.H. (2002) Helix-loop-helix proteins regulate pre-TCR and TCR signaling through modulation of Rel/NF-κB activities. Immunity 16, 9-21.
5. Mora, A.L., Stanley, S., Armistead, W., Chan, A.C. & Boothby, M. (2001) Inefficient ZAP-70 phosphorylation and decreased thymic selection in vivo result from inhibition of NF-κB/Rel. J. Immunol. 167, 5628-5635.
6. Brown, K., Gerstberger, S., Carlson, L., Franzoso, G. & Siebenlist, U. (1995) Control of IκB-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267, 1485-1488.
7. Fujimoto, K., Yasuda, H., Sato, Y. & Yamamoto, K. (1995) A role for phosphorylation in the proteolytic processing of the human NF-κB1 precursor. Gene 165, 183-189.
8. Naumann, M. & Scheidereit, C. (1994) Activation of NF-κB in vivo is regulated by multiple phosphorylations. EMBO J. 13, 4597-4607.
9. Mosialos, G., Hamer, P., Capobianco, A.J., Laursen, R.A. & Gilmore, T.D. (1991) A protein kinase-A recognition sequence is structurally linked to transformation by p59v-rel and cytoplasmic retention of p68c-rel. Mol. Cell Biol. 11, 5867-5877.
10. Ghosh, S. & Baltimore, D. (1990) Activation in vitro of NF-κB by phosphorylation of its inhibitor IκB. Nature 344, 678-682.
11. Zhong, H., SuYang, H., Erdjument-Bromage, H., Tempst, P. & Ghost, 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.
12. Zhong, H., Voll, R.E. & Ghosh, S. (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, 661-671.
13. Zhong, H., May, M.J., Jimi, E. & Ghosh, S. (2002) The Phosphorylation status of nuclear NF-κB determines its association with CBP/p300 or HDAC-1. Mol. Cell 9, 625-636.
14. Hayashi, T., Sekine, T. & Okamoto, T. (1993) Identification of a new serine kinase that activates NFκB by direct phosphorylation. J. Biol. Chem. 268, 26790-26795.
15. Schmid, R.M., Perkins, N.D., Duckett, C.S., Andrews, P.C. & Nabel, G.J. (1991) Cloning of an NF-κB subunit which stimulates HIV transcription in synergy with p65. Nature 352, 733-736.
16. Hofmann, F., Ammendola, A. & Schlossmann, J. (2000) Rising behind NO: cGMP-dependent protein kinases. J. Cell Sci. 113, 1671-1676.
17. Ruth, P. (1999) Cyclic GMP-dependent protein kinases: understanding in vivo functions by gene targeting. Pharmacol. Ther. 82, 355-372.
18. Weber, G.F. (1999) Final common pathways in neurodegenerative diseases: regulatory role of the glutathione cycle. Neurosci. Biobehav. Rev. 23, 1079-1086.
19. Chiche, J.D., Schlutsmeyer, S.M., Bloch, D.B., de la Monte, S.M., Roberts, J.D. Jr, Filippov, G., Janssens, S.P., Rosenzweig, A. & Bloch, K.D. (1998) Adenovirus-mediated gene transfer of cGMP-dependent protein kinase increases the sensitivity of cultured vascular smooth muscle cells to the antiproliferative and proapoptotic effects of nitric oxide/cGMP. J. Biol. Chem. 273, 34263-34271.
20. Loweth, A.C., Williams, G.T., Scarpello, J.H. & Morgan, N.G. (1997) Evidence for the involvement of cGMP and protein kinase G in nitric oxide-induced apoptosis in the pancreatic B-cell line, HIT-T15. FEBS Lett. 400, 285-288.
21. Taimor, G., Hofstaetter, B. & Piper, H.M. (2000) Apoptosis induction by nitric oxide in adult cardiomyocytes via cGMP-signaling and its impairment after simulated ischemia. Cardiovasc. Res. 45, 588-594.
22. Weber, G.F. (2002) Altered lymphocyte calcium signaling and age-related diseases. In Calcium Homeostasis and Signaling in Aging. Advances in Cell Aging and Gerontology, Vol. 10 (Mattson, M.P., ed), pp. 127-145. Elsevier, Amsterdam.
23. Takuma, K., Phuagphong, P., Lee, E., Mori, K., Baba, A. & Matsuda, T. (2001) Anti-apoptotic effect of cGMP in cultured astrocytes: inhibition by cGMP-dependent protein kinase of mitochondrial permeable transition pore. J. Biol. Chem. 276, 48093-48099.
24. Canals, S., Casarejos, M.J., de Bernardo, S., Rodrignez-Martin, E. & Mena, M.A. (2001) Glutathione depletion switches nitric oxide neurotrophic effects to cell death in midbrain cultures: implications for Parkinson's disease. J. Neurochem. 79, 1183-1195.
25. Liu, L., Li, H., Underwood, T., Lloyd, M., David, M., Sperl, G., Pamukcu, R. & Thompson, W.J. (2001) Cyclic GMP-dependent protein kinase activation and induction by exisulind and CP461 in colon tumor cells. J. Pharmacol. Exp. Ther. 299, 583-592.
26. Piazza, G.A., Thompson, W.J., Pamukcu, R., Alila, H.W., Whitehead, C.M., Liu, L., Fetter, J.R., Gresh, W.E. Jr, Klein-Szanto, A.J., Farnell, D.R., Eto, I. & Grubbs, C.J. (2001) Exisulind, a novel proapoptotic drug, inhibits rat urinary bladder tumorigenesis. Cancer Res. 61, 3961-3968.
27. Thompson, W.J., Piazza, G.A., Li, H., Liu, L., Fetter, J., Zhu, B., Sperl, G., Ahnen, D. & Pamukcu, R. (2000) Exisulind induction of apoptosis involves guanosine 3′,5′-cyclic monophosphate phosphodiesterase inhibition, protein kinase G activation, and attenuated beta-catenin. Cancer Res. 60, 3338-3342.
28. Wong, A.S., Kim, S.O., Leung, P.C., Auersperg, N. & Pelech, S.L. (2001) Profiling of protein kinases in the neoplastic transformation of human ovarian surface epithelium. Gynecol. Oncol. 82, 305-311.
29. Gudi, T., Lohmann, S.M. & Pilz, R.B. (1997) Regulation of gene expression by cyclic GMP-dependent protein kinase requires nuclear translocation of the kinase: identification of a nuclear localization signal. Mol. Cell Biol. 17, 5244-5254.
30. Gudi T., Casteel, D.E., Vinson, C., Boss, G.R. & Pilz, R.B. (2000) NO activation of fos promoter elements requires nuclear translocation of G-kinase I and CREB phosphorylation but is independent of MAP kinase activation. Oncogene 19, 6324-6333.
31. Friedman, S., Sillcocks, D. & Cantor, H. (1987) Alloreactivity of an OVA-specific T-cell clone. I. Stimulation by class II MHC and novel non-MHC B-cell determinants. Immunogenetics 26, 193-203.
32. Weber, G.F. & Cantor, H. (1994) Phosphatidylinositol synthesis is a proximal event in intracellular signalling coupled to T-cell receptor ligation: Differential induction by conventional antigen and superantigen. J. Immunol. 152, 4433-4443.
33. b) mice. J. Immunol. 138, 3991-3995.
34. + lymphocytes. Science 256, 1452-1456.
35. Cha-Molstad, H., Agrawal, A., Zhang, D., Samols, D. & Kushner, I. (2000) The Rel family member P50 mediates cytokine-induced C-reactive protein expression by a novel mechanism. J. Immunol. 165, 4592-4597.
36. Agrawal, A., Cha-Molstad, H., Samols, D. & Kushner, I. (2001) Transactivation of C-reactive protein by IL-6 requires synergistic interaction of CCAAT/enhancer binding protein beta (C/EBP beta) and Rel p50. J. Immunol. 166, 2378-2384.
37. Proesch, S., Heine, A.K., Volk, H.-D. & Krueger, D.H. (2001) CCAAT/enhancer binding proteins α and β negatively influence the capacity of tumor necrosis factor α to up-regulate the human cytomegalovirus IE1/2 enhancer/promoter by nuclear factor κB during monocyte differentiation. J. Biol. Chem. 276, 40712-40720.
38. Bours, V., Franzoso, G., Azarenko, V., Park, S., Kanno, T., Brown, K. & Siebenlist, U. (1993) The oncoprotein Bcl-3 directly transactivates through κB motifs via association with DNA-binding p50B homodimers. Cell 72, 729-739.
39. Liptay, S., Schmid, R.M., Perkins, N.D., Meltzer, P., Altherr, M.R., McPherson, J.D., Wasmuth, J.J. & Nabel, G.J. (1992) Related subunits of NF-κB map to two distinct loci associated with translocations in leukemia, NFKB1 and NFKB2. Genomics 13, 287-292.
40. Kim, T.K. & Maniatis, T. (1997) The mechanism of transcriptional synergy of an in vitro assembled interferon-β enhanceosome. Mol. Cell 1, 119-129.
41. Perkins, N.D., Schmid, R.M., Duckett, C.S., Leung, K., Rice, N.R. & Nabel, G.J. (1992) Distinct combinations of NF-κB subunits determine the specificity of transcriptional activation. Proc. Natl Acad. Sci. USA 89, 1529-1533.
42. Gudi, T., Huvar, I., Meinecke, M., Lohmann, S.M., Boss, G.R. & Pilz, R.B. (1996) Regulation of gene expression by cGMP-dependent protein kinase. J. Biol. Chem. 271, 4597-4600.