Abstract
NF-kappaB signaling is known to be critically regulated by the NF-kappaB-inducible inhibitor protein IkappaBalpha. The resulting negative feedback has been shown to produce a propensity for oscillations in NF-kappaB activity. We report integrated experimental and computational studies that demonstrate that another IkappaB isoform, IkappaBepsilon, also provides negative feedback on NF-kappaB activity, but with distinct functional consequences. Upon stimulation, NF-kappaB-induced transcription of IkappaBepsilon is delayed, relative to that of IkappaBalpha, rendering the two negative feedback loops to be in antiphase. As a result, IkappaBepsilon has a role in dampening IkappaBalpha-mediated oscillations during long-lasting NF-kappaB activity. Furthermore, we demonstrate the requirement of both of these distinct negative feedback regulators for the termination of NF-kappaB activity and NF-kappaB-mediated gene expression in response to transient stimulation. Our findings extend the capabilities of a computational model of IkappaB-NF-kappaB signaling and reveal a novel regulatory module of two antiphase negative feedback loops that allows for the fine-tuning of the dynamics of a mammalian signaling pathway.
MeSH Terms
Animals
Biological Clocks/physiology
Cell Line
Cells, Cultured
Computer Simulation
Feedback, Physiological
Fibroblasts/metabolism
Gene Expression Regulation/drug effects
I-kappa B Proteins/drug effects,metabolism,pharmacology
Inflammation/genetics
Mice
NF-kappa B/analysis,genetics,metabolism
Signal Transduction/drug effects,physiology
Tumor Necrosis Factor-alpha/pharmacology
Chemicals
I-kappa B Proteins
NF-kappa B
Tumor Necrosis Factor-alpha
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Kearns Jeffrey D
Signaling Systems Laboratory, Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, CA 92093, USA.
Basak Soumen
Werner Shannon L
Huang Christine S
Hoffmann Alexander
References (21)
21 references, click to expand
-
IkappaBepsilon-deficient mice: reduction of one T cell precursor subspecies and enhanced Ig isotype switching and cytokine synthesis.
J Immunol. 1999 Dec 1;163(11):5994-6005
PMID: 10570287
-
Circuitry of nuclear factor kappaB signaling.
Immunol Rev. 2006 Apr;210:171-86
PMID: 16623771
-
A functional role of I kappa B-epsilon in endothelial cell activation.
J Immunol. 2000 Mar 15;164(6):3316-22
PMID: 10706725
-
NF-kappaB regulation in the immune system.
Nat Rev Immunol. 2002 Oct;2(10):725-34
PMID: 12360211
-
The IkappaB-NF-kappaB signaling module: temporal control and selective gene activation.
Science. 2002 Nov 8;298(5596):1241-5
PMID: 12424381
-
Genetic analysis of NF-kappaB/Rel transcription factors defines functional specificities.
EMBO J. 2003 Oct 15;22(20):5530-9
PMID: 14532125
-
Inactivating I kappa B epsilon mutations in Hodgkin/Reed-Sternberg cells.
J Pathol. 2003 Nov;201(3):413-20
PMID: 14595753
-
The IKK/NF-kappaB activation pathway-a target for prevention and treatment of cancer.
Cancer Lett. 2004 Apr 8;206(2):193-9
PMID: 15013524
-
Oscillations in NF-kappaB signaling control the dynamics of gene expression.
Science. 2004 Oct 22;306(5696):704-8
PMID: 15499023
-
The p65 subunit of NF-kappa B regulates I kappa B by two distinct mechanisms.
Genes Dev. 1993 Jul;7(7A):1266-76
PMID: 8319912
-
Role of unphosphorylated, newly synthesized I kappa B beta in persistent activation of NF-kappa B.
Mol Cell Biol. 1996 Oct;16(10):5444-9
PMID: 8816457
-
I kappa B epsilon, a novel member of the I kappa B family, controls RelA and cRel NF-kappa B activity.
EMBO J. 1997 Mar 17;16(6):1413-26
PMID: 9135156
-
Regulation of IkappaB beta in WEHI 231 mature B cells.
Mol Cell Biol. 1997 Aug;17(8):4390-6
PMID: 9234697
-
Cloning and functional characterization of mouse IkappaBepsilon.
Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14372-7
PMID: 9405619
-
NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses.
Annu Rev Immunol. 1998;16:225-60
PMID: 9597130
-
Reductions in I kappa B epsilon and changes in NF-kappa B activity during B lymphocyte differentiation.
J Immunol. 2005 Jan 15;174(2):983-91
PMID: 15634922
-
Comment on "Oscillations in NF-kappaB signaling control the dynamics of gene expression".
Science. 2005 Apr 1;308(5718):52; author reply 52
PMID: 15802586
-
Inflammation-associated cancer: NF-kappaB is the lynchpin.
Trends Immunol. 2005 Jun;26(6):318-25
PMID: 15922948
-
Achieving stability of lipopolysaccharide-induced NF-kappaB activation.
Science. 2005 Sep 16;309(5742):1854-7
PMID: 16166516
-
Stimulus specificity of gene expression programs determined by temporal control of IKK activity.
Science. 2005 Sep 16;309(5742):1857-61
PMID: 16166517
-
Genetic approaches in mice to understand Rel/NF-kappaB and IkappaB function: transgenics and knockouts.
Oncogene. 1999 Nov 22;18(49):6888-95
PMID: 10602464