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Science 306 (5696): 704-708

Copyright © 2004 by the American Association for the Advancement of Science

Oscillations in NF-{kappa}B Signaling Control the Dynamics of Gene Expression

D. E. Nelson,1 A. E. C. Ihekwaba,2 M. Elliott,1 J. R. Johnson,1 C. A. Gibney,1 B. E. Foreman,1 G. Nelson,1 V. See,1 C. A. Horton,1 D. G. Spiller,1 S. W. Edwards,1 H. P. McDowell,4 J. F. Unitt,5 E. Sullivan,6 R. Grimley,7 N. Benson,7 D. Broomhead,3 D. B. Kell,2 M. R. H. White1*

Abstract: Signaling by the transcription factor nuclear factor kappa B (NF-{kappa}B) involves its release from inhibitor kappa B (I{kappa}B) in the cytosol, followed by translocation into the nucleus. NF-{kappa}B regulation of I{kappa}B{alpha} transcription represents a delayed negative feedback loop that drives oscillations in NF-{kappa}B translocation. Single-cell time-lapse imaging and computational modeling of NF-{kappa}B (RelA) localization showed asynchronous oscillations following cell stimulation that decreased in frequency with increased I{kappa}B{alpha} transcription. Transcription of target genes depended on oscillation persistence, involving cycles of RelA phosphorylation and dephosphorylation. The functional consequences of NF-{kappa}B signaling may thus depend on number, period, and amplitude of oscillations.

1 Centre for Cell Imaging, School of Biological Sciences, Bioscience Research Building, Crown Street, Liverpool, L69 7ZB, UK.
2 Department of Chemistry, University of Manchester Institute of Science and Technology, P.O. Box 88, Sackville Street, Manchester, M60 1QD, UK.
3 Department of Mathematics, University of Manchester Institute of Science and Technology, P.O. Box 88, Sackville Street, Manchester, M60 1QD, UK.
4 Royal Liverpool Children's National Health Service Trust, Alder Hey Hospital, Eaton Road, Liverpool, L12 2AP, UK.
5 Molecular Biology Department, AstraZeneca Research and Development Charnwood, Bakewell Road, Loughborough, Leicestershire, LE11 5RH, UK.
6 Advanced Science and Technology Laboratory, AstraZeneca Research and Development Charnwood, Bakewell Road, Loughborough, Leicestershire, LE11 5RH, UK.
7 Pfizer Central Research, Ramsgate Road, Sandwich, Kent, CT13 9NJ, UK.

* To whom correspondence should be addressed. E-mail: mwhite{at}liv.ac.uk

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Inducible Phosphorylation of NF-{kappa}B p65 at Serine 468 by T Cell Costimulation Is Mediated by IKK{epsilon}.
I. Mattioli, H. Geng, A. Sebald, M. Hodel, C. Bucher, M. Kracht, and M. L. Schmitz (2006)
J. Biol. Chem. 281, 6175-6183
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Tumor Necrosis Factor-{alpha} Activates the Human Prolactin Gene Promoter via Nuclear Factor-{kappa}B Signaling.
S. Friedrichsen, C. V. Harper, S. Semprini, M. Wilding, A. D. Adamson, D. G. Spiller, G. Nelson, J. J. Mullins, M. R. H. White, and J. R. E. Davis (2006)
Endocrinology 147, 773-781
   Abstract »    Full Text »    PDF »
Host and parasite-derived IKK activities direct distinct temporal phases of NF-{kappa}B activation and target gene expression following Toxoplasma gondii infection.
R. E. Molestina and A. P. Sinai (2005)
J. Cell Sci. 118, 5785-5796
   Abstract »    Full Text »    PDF »
Prevention of NF-{kappa}B activation in vivo by a cell-permeable NF-{kappa}B inhibitor peptide.
A. L. Mora, J. LaVoy, M. McKean, A. Stecenko, K. L. Brigham, R. Parker, and M. Rojas (2005)
Am J Physiol Lung Cell Mol Physiol 289, L536-L544
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Achieving Stability of Lipopolysaccharide-Induced NF-{kappa}B Activation.
M. W. Covert, T. H. Leung, J. E. Gaston, and D. Baltimore (2005)
Science 309, 1854-1857
   Abstract »    Full Text »    PDF »
Stimulus Specificity of Gene Expression Programs Determined by Temporal Control of IKK Activity.
S. L. Werner, D. Barken, and A. Hoffmann (2005)
Science 309, 1857-1861
   Abstract »    Full Text »    PDF »
Systems biology in the cell nucleus.
S. Gorski and T. Misteli (2005)
J. Cell Sci. 118, 4083-4092
   Abstract »    Full Text »    PDF »
Coactivators and Corepressors of NF-{kappa}B in I{kappa}B{alpha} Gene Promoter.
Z. Gao, P. Chiao, X. Zhang, X. Zhang, M. A. Lazar, E. Seto, H. A. Young, and J. Ye (2005)
J. Biol. Chem. 280, 21091-21098
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