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J. Biol. Chem., Vol. 276, Issue 34, 32080-32093, August 24, 2001
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From the NF-
NF-
B-inducible BCL-3 Expression Is an
Autoregulatory Loop Controlling Nuclear p50/NF-B1 Residence*
§,,,, and Departments of Internal Medicine and Human
Biological Chemistry and Genetics and the ¶ Department of
Microbiology and Immunology, the University of Texas Medical Branch,
Galveston, Texas 77555-1060
B is a transcription factor whose nuclear
residence is controlled by IB family members. In the NF-B-IB
autoregulatory loop, activated (nuclear) Rel A·NF-B1 induces the
resynthesis of IB
recapturing nuclear Rel A back into the
cytoplasm within 1 h of stimulation. In contrast, NF-B1
subunits redistribute more slowly into the cytoplasm (from 6 to 12 h). Here we examine the role of inducible cytoplasmic BCL-3 expression
in terminating nuclear NF-B1. Although BCL-3 is a nuclear protein in
B lymphocytes, surprisingly, BCL-3 is primarily a cytoplasmic protein
in HepG2 cells. Cytoplasmic BCL-3 abundance is induced 6-12 h after
tumor necrosis factor- stimulation where it complexes with NF-B1
homodimers. Moreover, BCL-3 mRNA and protein expression are induced
by NF-B-activating agents. Two observations are interpreted to
indicate that bcl-3 is transactivated by NF-B/Rel A: 1)
expression of a dominant negative NF-B inhibitor blocks tumor
necrosis factor--induced BCL-3 expression and 2) expression of
constitutively active Rel A is sufficient to induce BCL-3 expression.
In gene transfer studies, we identify two high affinity NF-B-binding
sites, B1 (located at 
872 to 861 nucleotides) and B2 (106
to 96 nucleotides), and although both bind with high affinity to Rel
A, only B2 is required for NF-B-dependent induction
of the native BCL-3 promoter. Down-regulation of
BCL-3 induction results in prolonged, enhanced NF-B1 binding and
increased NF-B-dependent transcription. Together, these
data suggest the presence of an NF-B-BCL-3 autoregulatory loop
important in terminating NF-B1 action and that individual NF-B
isoforms are actively terminated through coordinate induction of
inhibitory IB molecules to restore cellular homeostasis.
*
This work was supported in part by NHLBI Grant 55630 from
the National Institutes of Health (to A. R. B.), American Heart Association Grant-in-aid 9950345N, and NIEHS Grant ES06676 from the
National Institutes of Health (to R. S. Lloyd, University of Texas
Medical Branch). This work was presented in part in abstract form at
the American Society for Molecular Biology Annual Meeting, June
4-8, 2000, Boston, MA.The costs of publication of this
article were defrayed in part by the
payment of page charges. The article must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
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