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research
Distinct Mechanisms for Induction and Tolerance Regulate the Immediate Early Genes Encoding Interleukin 1β and Tumor Necrosis Factor α
Authors
A Barski
A Barski
+87 more
A Morotti
AJ Donner
An-Jey A. Su
AR Brasier
B Grondin
BL Ebert
BN Devaiah
C Hagemeier
C Jiang
C-Y Chen
CA Dinarello
CA Dinarello
Chunhong Yan
CK Lee
DA Gilchrist
DA Gilchrist
DC Hargreaves
DE Schones
Deborah L. Galson
DJ Van Antwerp
DL Galson
DV Kuprash
E Kowenz-Leutz
F Sandor
F Shirakawa
F Shirakawa
G Natoli
Gillian M. Tannahill
GM Tannahill
GM Tannahill
GW Muse
HT Kang
J Dekker
J Dekker
J Hiscott
J Tsukada
J Tsukada
J Xie
JA Listman
JM Argiles
Juraj Adamik
K Adelman
Kent Z. Q. Wang
KJ Meaburn
KZ Wang
L Bai
L Escoubet-Lozach
LJ Core
Luke A. O’Neill
M Kronke
M Vermeulen
MA Collart
MG Guenther
MJ Fenton
MO Hottiger
N Wara-aswapati
NS Kenneth
PE Auron
Philip E. Auron
Q Zhou
RC Akkers
S Egloff
S Ghisletti
S Heinz
S Henikoff
S Marecki
S Marmiroli
S Mink
S Unlu
SA Godambe
Sebnem Unlu
SH Zuckerman
SJ Petesch
SK Roy
SL Foster
SN Sarkar
SP Davies
T Lawrence
T Mitchell
T Tando
TN Mavrich
W Deng
X Contreras
Y Kominato
Y Yoshida
Z Yang
Z Yang
Publication date
1 January 2013
Publisher
'Public Library of Science (PLoS)'
Doi
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on
PubMed
Abstract
Interleukin-1β and Tumor Necrosis Factor α play related, but distinct, roles in immunity and disease. Our study revealed major mechanistic distinctions in the Toll-like receptor (TLR) signaling-dependent induction for the rapidly expressed genes (IL1B and TNF) coding for these two cytokines. Prior to induction, TNF exhibited pre-bound TATA Binding Protein (TBP) and paused RNA Polymerase II (Pol II), hallmarks of poised immediate-early (IE) genes. In contrast, unstimulated IL1B displayed very low levels of both TBP and paused Pol II, requiring the lineage-specific Spi-1/PU.1 (Spi1) transcription factor as an anchor for induction-dependent interaction with two TLR-activated transcription factors, C/EBPβ and NF-κB. Activation and DNA binding of these two pre-expressed factors resulted in de novo recruitment of TBP and Pol II to IL1B in concert with a permissive state for elongation mediated by the recruitment of elongation factor P-TEFb. This Spi1-dependent mechanism for IL1B transcription, which is unique for a rapidly-induced/poised IE gene, was more dependent upon P-TEFb than was the case for the TNF gene. Furthermore, the dependence on phosphoinositide 3-kinase for P-TEFb recruitment to IL1B paralleled a greater sensitivity to the metabolic state of the cell and a lower sensitivity to the phenomenon of endotoxin tolerance than was evident for TNF. Such differences in induction mechanisms argue against the prevailing paradigm that all IE genes possess paused Pol II and may further delineate the specific roles played by each of these rapidly expressed immune modulators. © 2013 Adamik et al
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