Regulation of c-Rel Nuclear Localization by Binding of Ca²⁺/Calmodulin

REFERENCES

• Arenzana Seisdedos, F., P. Turpin, M. Rodriguez, D. Thomas, R. T. Hay, J. L. Virelizier, and C. Dargemont. 1997. Nuclear localization of I kappa B alpha promotes active transport of NF-kappa B from the nucleus to the cytoplasm. J. Cell Sci. 110: 369–378.
   PubMedGoogle Scholar
• Barkett, M., and T. D. Gilmore. 1999. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18: 6910–6924.
   PubMed Web of Science ®Google Scholar
• 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 I kappa B alpha: a mechanism for NF-kappa B activation. Mol. Cell. Biol. 13: 3301–3310.
   PubMed Web of Science ®Google Scholar
• Bird, T. A., K. Schooley, S. K. Dower, H. Hagen, and G. D. Virca. 1997. Activation of nuclear transcription factor NF-kappaB by interleukin-1 is accompanied by casein kinase II-mediated phosphorylation of the p65 subunit. J. Biol. Chem. 272: 32606–32612.
   PubMed Web of Science ®Google Scholar
• Capobianco, A. J., D. L. Simmons, and T. D. Gilmore. 1990. Cloning and expression of a chicken c-rel cDNA: unlike p59v-rel, p68c-rel is a cytoplasmic protein in chicken embryo fibroblasts. Oncogene 5: 257–265.
   PubMedGoogle Scholar
• Carafoli, E., P. Nicotera, and L. Santella. 1997. Calcium signalling in the cell nucleus. Cell Calcium 22: 313–319.
   PubMedGoogle Scholar
• Chen, F. E., and G. Ghosh. 1999. Regulation of DNA binding by Rel/NF-kappaB transcription factors: structural views. Oncogene 18: 6845–6852.
   PubMed Web of Science ®Google Scholar
• Cockerill, P. N., M. F. Shannon, A. G. Bert, G. R. Ryan, and M. A. Vadas. 1993. The granulocyte-macrophage colony-stimulating factor/interleukin 3 locus is regulated by an inducible cyclosporin A-sensitive enhancer. Proc. Natl. Acad. Sci. USA 90: 2466–2470.
   PubMed Web of Science ®Google Scholar
• Conti, E., M. Uy, L. Leighton, G. Blobel, and J. Kuriyan. 1998. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell 94: 193–204.
   PubMed Web of Science ®Google Scholar
• Corneliussen, B., M. Holm, Y. Waltersson, J. Onions, B. Hallberg, A. Thornell, and T. Grundstrüm. 1994. Calcium/calmodulin inhibition of basic-helix-loop-helix transcription factor domains. Nature 368: 760–764.
   PubMed Web of Science ®Google Scholar
• Doerre, S., P. Sista, S. C. Sun, D. W. Ballard, and W. C. Greene. 1993. The c-rel protooncogene product represses NF-kappa B p65-mediated transcriptional activation of the long terminal repeat of type 1 human immunodeficiency virus. Proc. Natl. Acad. Sci. USA 90: 1023–1027.
   PubMedGoogle Scholar
• Dolmetsch, R. E., R. S. Lewis, C. C. Goodnow, and J. I. Healy. 1997. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386: 855–858.
   PubMed Web of Science ®Google Scholar
• Dolmetsch, R. E., K. Xu, and R. S. Lewis. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392: 933–936.
   PubMedGoogle Scholar
• Durand, D. B., J. P. Shaw, M. R. Bush, R. E. Replogle, R. Belagaje, and G. R. Crabtree. 1988. Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol. Cell. Biol. 8: 1715–1724.
   PubMed Web of Science ®Google Scholar
• Gerondakis, S., M. Grossmann, Y. Nakamura, T. Pohl, and R. Grumont. 1999. Genetic approaches in mice to understand Rel/NF-kappaB and IkappaB function: transgenics and knockouts. Oncogene 18: 6888–6895.
   PubMed Web of Science ®Google Scholar
• Gerritsen, M. E., A. J. Williams, A. S. Neish, S. Moore, Y. Shi, and T. Collins. 1997. CREB-binding protein/p300 are transcriptional coactivators of p65. Proc. Natl. Acad. Sci. USA 94: 2927–2932.
   PubMed Web of Science ®Google Scholar
• Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl.): S81–S96.
   PubMed Web of Science ®Google Scholar
• Ghosh, S., M. J. May, and E. B. Kopp. 1998. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225–260.
   PubMed Web of Science ®Google Scholar
• Govind, S. 1999. Control of development and immunity by Rel transcription factors in Drosophila. Oncogene 18: 6875–6887.
   PubMedGoogle Scholar
• Harhaj, E. W., and S. C. Sun. 1999. Regulation of RelA subcellular localization by a putative nuclear export signal and p50. Mol. Cell. Biol. 19: 7088–7095.
   PubMedGoogle Scholar
• Harley, V. R., R. Lovell Badge, P. N. Goodfellow, and P. J. Hextall. 1996. The HMG box of SRY is a calmodulin binding domain. FEBS Lett. 391: 24–28.
   PubMed Web of Science ®Google Scholar
• Hermann, S., J. Saarikettu, J. Onions, K. Hughes, and T. Grundstrom. 1998. Calcium regulation of basic helix-loop-helix transcription factors. Cell Calcium 23: 135–142.
   PubMedGoogle Scholar
• Huang, T. T., N. Kudo, M. Yoshida, and S. Miyamoto. 2000. A nuclear export signal in the N-terminal regulatory domain of IkappaBalpha controls cytoplasmic localization of inactive NF-kappaB/IkappaBalpha complexes. Proc. Natl. Acad. Sci. USA 97: 1014–1019.
   PubMed Web of Science ®Google Scholar
• Hughes, K., Å. Antonsson, and T. Grundstrüm. 1998. Calmodulin dependence of NFkappaB activation. FEBS Lett. 441: 132–136.
   PubMedGoogle Scholar
• Hughes, K., S. Edin, A. Antonsson, and T. Grundstrom. 2001. Calmodulin-dependent kinase II mediates T cell receptor/CD3- and phorbol ester-induced activation of IkappaB kinase. J. Biol. Chem. 276: 36008–36013.
   PubMedGoogle Scholar
• Ikura, M., G. M. Clore, A. M. Gronenborn, G. Zhu, C. B. Klee, and A. Bax. 1992. Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256: 632–638.
   PubMed Web of Science ®Google Scholar
• Israel, A. 2000. The IKK complex: an integrator of all signals that activate NF-kappaB? Trends Cell Biol. 10: 129–133.
   PubMed Web of Science ®Google Scholar
• Jacobs, M. D., and S. C. Harrison. 1998. Structure of an IkappaBalpha/NF-kappaB complex. Cell 95: 749–758.
   PubMed Web of Science ®Google Scholar
• Jain, J., C. Loh, and A. Rao. 1995. Transcriptional regulation of the IL-2 gene. Curr. Opin. Immunol. 7: 333–342.
   PubMed Web of Science ®Google Scholar
• Johnson, C., D. Van Antwerp, and T. J. Hope. 1999. An N-terminal nuclear export signal is required for the nucleocytoplasmic shuttling of IkappaBalpha. EMBO J. 18: 6682–6693.
   PubMed Web of Science ®Google Scholar
• Karin, M. 1999. How NF-kappaB is activated: the role of the IkappaB kinase (IKK) complex. Oncogene 18: 6867–6874.
   PubMed Web of Science ®Google Scholar
• Karin, M., and M. Delhase. 2000. The I kappa B kinase (IKK) and NF-kappa B: key elements of proinflammatory signalling. Semin. Immunol. 12: 85–98.
   PubMed Web of Science ®Google Scholar
• Kim, B. C., H. T. Kim, M. Mamura, I. S. Ambudkar, K. S. Choi, and S. J. Kim. 2002. TNF induces apoptosis in hepatoma cells by increasing Ca2+ release from the endoplasmic reticulum and suppressing Bcl-2 expression. J. Biol. Chem. 277: 31381–31389.
   PubMed Web of Science ®Google Scholar
• Lahdenpohja, N., T. Henttinen, and M. Hurme. 1996. Activation of the protein kinase A increases the DNA-binding and transcriptional activity of c-Rel in T cells. Scand. J. Immunol. 43: 640–645.
   PubMedGoogle Scholar
• Lars, N., and S. Paschalis. 1993. The human I alpha 1 and I alpha 2 germline promoter elements: proximal positive and distal negative elements may regulate the tissue specific expression of C alpha 1 and C alpha 2 germline transcripts. Int. Immunol. 5: 271–282.
   PubMedGoogle Scholar
• Lenardo, M. J., A. Kuang, A. Gifford, and D. Baltimore. 1988. NF-kappa B protein purification from bovine spleen: nucleotide stimulation and binding site specificity. Proc. Natl. Acad. Sci. USA 85: 8825–8829.
   PubMedGoogle Scholar
• Li, C. C., R. M. Dai, E. Chen, and D. L. Longo. 1994. Phosphorylation of NF-KB1-p50 is involved in NF-kappa B activation and stable DNA binding. J. Biol. Chem. 269: 30089–30092.
   PubMedGoogle Scholar
• Liljeholm, S., K. Hughes, T. Grundstrüm, and P. Brodin. 1998. NF-kappaB only partially mediates Epstein-Barr virus latent membrane protein 1 activation of B cells. J. Gen. Virol. 79: 2117–2125.
   PubMedGoogle Scholar
• MacEwan, D. J. 2002. TNF receptor subtype signalling: differences and cellular consequences. Cell. Signal. 14: 477–492.
   PubMed Web of Science ®Google Scholar
• Martin, A. G., and M. Fresno. 2000. Tumor necrosis factor-alpha activation of NF-kappa B requires the phosphorylation of Ser-471 in the transactivation domain of c-Rel. J. Biol. Chem. 275: 24383–24391.
   PubMedGoogle Scholar
• May, M. J., and S. Gosh. 1999. I-kappaB kinases: kinsmen with different crafts. Science 284: 271–273.
   PubMed Web of Science ®Google Scholar
• Meador, W. E., A. R. Means, and F. A. Quiocho. 1993. Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures. Science 262: 1718–1721.
   PubMed Web of Science ®Google Scholar
• Meador, W. E., A. R. Means, and F. A. Quiocho. 1992. Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulin-peptide complex. Science 257: 1251–1255.
   PubMed Web of Science ®Google Scholar
• Molitor, J. A., W. H. Walker, S. Doerre, D. W. Ballard, and W. C. Greene. 1990. NF-kappa B: a family of inducible and differentially expressed enhancer-binding proteins in human T cells. Proc. Natl. Acad. Sci. USA 87: 10028–10032.
   PubMed Web of Science ®Google Scholar
• Mosialos, G., P. Hamer, A. J. Capobianco, R. A. Laursen, and T. D. Gilmore. 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.
   PubMedGoogle Scholar
• Naumann, M., and C. Scheidereit. 1994. Activation of NF-kappa B in vivo is regulated by multiple phosphorylations. EMBO J. 13: 4597–4607.
   PubMed Web of Science ®Google Scholar
• Ning, Y. M., and E. R. Sanchez. 1995. Evidence for a functional interaction between calmodulin and the glucocorticoid receptor. Biochem. Biophys. Res. Commun. 208: 48–54.
   PubMedGoogle Scholar
• O'Neil, K. T., and W. F. DeGrado. 1990. How calmodulin binds its targets: sequence independent recognition of amphiphilic alpha-helices. Trends Biochem. Sci. 15: 59–64.
   PubMed Web of Science ®Google Scholar
• Onions, J., S. Hermann, and T. Grundstrüm. 1997. Basic helix-loop-helix protein sequences determining differential inhibition by calmodulin and S-100 proteins. J. Biol. Chem. 272: 23930–23937.
   PubMedGoogle Scholar
• Pahl, H. L. 1999. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853–6866.
   PubMed Web of Science ®Google Scholar
• Parry, G. C., and N. Mackman. 1997. Role of cyclic AMP response element-binding protein in cyclic AMP inhibition of NF-kappaB-mediated transcription. J. Immunol. 159: 5450–5456.
   PubMed Web of Science ®Google Scholar
• Perkins, N. D. 1997. Achieving transcriptional specificity with NF-kappa B. Int. J. Biochem. Cell Biol. 29: 1433–1448.
   PubMed Web of Science ®Google Scholar
• Perkins, N. D., L. K. Felzien, J. C. Betts, K. Leung, D. H. Beach, and G. J. Nabel. 1997. Regulation of NF-kappaB by cyclin-dependent kinases associated with the p300 coactivator. Science 275: 523–527.
   PubMed Web of Science ®Google Scholar
• Rodriguez, M. S., J. Thompson, R. T. Hay, and C. Dargemont. 1999. Nuclear retention of I-kappaBalpha protects it from signal-induced degradation and inhibits nuclear factor kappaB transcriptional activation. J. Biol. Chem. 274: 9108–9115.
   PubMed Web of Science ®Google Scholar
• Sachdev, S., and M. Hannink. 1998. Loss of IkappaB alpha-mediated control over nuclear import and DNA binding enables oncogenic activation of c-Rel. Mol. Cell. Biol. 18: 5445–5456.
   PubMedGoogle Scholar
• Schmitz, M. L., S. Bacher, and M. Kracht. 2001. I kappa B-independent control of NF-kappa B activity by modulatory phosphorylations. Trends Biochem. Sci. 26: 186–190.
   PubMed Web of Science ®Google Scholar
• Schmitz, M. L., M. A. dos Santos Silva, and P. A. Baeuerle. 1995. Transactivation domain 2 (TA2) of p65 NF-kappa B. Similarity to TA1 and phorbol ester-stimulated activity and phosphorylation in intact cells. J. Biol. Chem. 270: 15576–15584.
   PubMed Web of Science ®Google Scholar
• Serfling, E., A. Avots, and M. Neumann. 1995. The architecture of the interleukin-2 promoter: a reflection of T lymphocyte activation Biochim. Biophys. Acta 1263: 181–200.
   PubMed Web of Science ®Google Scholar
• Shannon, M. F., L. S. Coles, M. A. Vadas, and P. N. Cockerill. 1997. Signals for activation of the GM-CSF promoter and enhancer in T cells. Crit. Rev. Immunol. 17: 301–323.
   PubMedGoogle Scholar
• Shen, C. H., and J. Stavnezer. 1998. Interaction of stat6 and NF-kappaB: direct association and synergistic activation of interleukin-4-induced transcription. Mol. Cell. Biol. 18: 3395–3404.
   PubMed Web of Science ®Google Scholar
• Szymanski, D. B., B. Liao, and R. E. Zielinski. 1996. Calmodulin isoforms differentially enhance the binding of cauliflower nuclear proteins and recombinant TGA3 to a region derived from the Arabidopsis Cam-3 promoter. Plant Cell 8: 1069–1077.
   PubMed Web of Science ®Google Scholar
• Tam, W. F., L. H. Lee, L. Davis, and R. Sen. 2000. Cytoplasmic sequestration of rel proteins by IkappaBalpha requires CRM1-dependent nuclear export. Mol. Cell. Biol. 20: 2269–2284.
   PubMedGoogle Scholar
• Tam, W. F., W. Wang, and R. Sen. 2001. Cell-specific association and shuttling of IkappaBalpha provides a mechanism for nuclear NF-kappaB in B lymphocytes. Mol. Cell. Biol. 21: 4837–4846.
   PubMedGoogle Scholar
• Thornell, A., B. Hallberg, and T. Grundstrom. 1988. Differential protein binding in lymphocytes to a sequence in the enhancer of the mouse retrovirus SL3-3. Mol. Cell. Biol. 8: 1625–1637.
   PubMedGoogle Scholar
• Van Eldik, L., and D. M. Watterson (ed.). 1998. Calmodulin and signal transduction. Academic Press, New York, N.Y.
   Google Scholar
• Wang, D., and A. S. Baldwin, Jr. 1998. Activation of nuclear factor-kappaB-dependent transcription by tumor necrosis factor-alpha is mediated through phosphorylation of RelA/p65 on serine 529. J. Biol. Chem. 273: 29411–29416.
   PubMedGoogle Scholar
• Zhong, H., H. SuYang, H. Erdjument Bromage, P. Tempst, and S. Ghosh. 1997. The transcriptional activity of NF-kappaB is regulated by the IkappaB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89: 413–424.
   PubMed Web of Science ®Google Scholar
• Zhong, H., R. E. Voll, and S. Ghosh. 1998. Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1: 661–671.
   PubMed Web of Science ®Google Scholar