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J Virol, February 1998, p. 1623-1626, Vol. 72, No. 2
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Essential Roles of NF-
B and C/EBP in the
Regulation of Intercellular Adhesion Molecule-1 after Respiratory
Syncytial Virus Infection of Human Respiratory Epithelial Cell
Cultures
B. A.
Chini,1
M. A.
Fiedler,2
L.
Milligan,2
T.
Hopkins,2 and
J.
M.
Stark2,*
Division of Pulmonary Medicine, Children's
Hospital, Pittsburgh, Pennsylvania,1 and
Division of Pulmonary Medicine, Children's Hospital Medical
Center, Cincinnati, Ohio2
Received 22 August 1997/Accepted 16 October 1997
 |
ABSTRACT |
To determine the molecular mechanism(s) of respiratory syncytial
virus (RSV)-induced intercellular adhesion molecule-1 (ICAM-1) upregulation in respiratory epithelial cells (REC; A549 cell cultures), we investigated the roles of the transcription factors NF-
B and C/EBP. Increases in ICAM-1 message required de novo mRNA synthesis. ICAM-1 promoter constructs (luciferase reporter gene) transfected into
A549 monolayers demonstrated promoter activation following RSV
infection. Activation was abolished by site-specific mutation of the
NF-B (
228) or C/EBP (239) sites. These data support the critical
role of the activation of NF-B and C/EBP in RSV-induced ICAM-1
expression by REC.
| |
TEXT |
Respiratory syncytial virus (RSV) is
the most important viral pathogen in infancy and early childhood
(11, 21). Animal models of RSV bronchiolitis demonstrate
acute airway obstruction associated with intense interstitial and
peribronchial infiltrates (10, 27), features that are
similar to observations in human autopsy specimens (1) and
lavage samples from infants with RSV (5, 20). Studies in
infants demonstrate that RSV infection causes production of a number of
cytokines (4, 19, 20). Moreover, infection of airway
epithelial cells by RSV upregulates the expression of intercellular
adhesion molecule-1 (ICAM-1) (25, 28). The role of ICAM-1 in
lung inflammation has been inferred from in vitro and in vivo studies
with monoclonal antibodies (23, 31) and substantiated by
studies of bronchial biopsies from asthmatics (18, 29). In
the context of respiratory virus infection, the production of
chemoattractive cytokines and ICAM-1 could provide a means of
recruiting and retaining inflammatory cells within the airway,
contributing to RSV-mediated lung injury.
Several groups have investigated the transcriptional regulation of the
ICAM-1 gene and demonstrated differences in tumor necrosis factor alpha
(TNF-
)- and gamma interferon (IFN-
)-induced upregulation of
ICAM-1 (13, 15, 16, 26, 30). RSV infection activates a
number of transcription factors in respiratory epithelial cell cultures
(6, 8, 17). The ICAM-1 promoter contains consensus binding
sequences for several of these factors, implying but not proving that
they contribute to virus-induced ICAM-1 activation. The studies
described here were designed to identify the molecular mechanism of
ICAM-1 gene activation following RSV infection in respiratory
epithelial cell cultures.
Effects of RSV infection on ICAM-1 mRNA.
Initial studies were
performed to examine ICAM-1 transcription following RSV infection. RNA
was prepared from RSV-infected and control A549 cells following RSV
exposure (RNeasy kit; Qiagen, Chatsworth, Calif.) and analyzed by
Northern blot analysis (22) as described previously, probing
with 32P-labeled cDNAs for ICAM-1 or 
-actin
(6, 7). These studies demonstrated a biphasic increase in
mRNA levels, which peaked at 2 h following RSV exposure, decreased
by 6 h, and increased again 24 h into infection (Fig.
1), similar to the biphasic activation of
interleukin 8 (IL-8) following RSV infection (7). The cause of this biphasic activation is unclear, but the late phase requires viral replication (7). In order to determine whether the
increase in mRNA resulted from new RNA or protein synthesis, cells were treated with actinomycin D (10 µg/ml) or cycloheximide (10 µg/ml). ICAM-1 mRNA was undetectable in RSV-infected cells following treatment with actinomycin D for 5 h, whereas cycloheximide treatment had no
effect on ICAM-1 mRNA (Fig. 2).
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FIG. 1.
Time course of RSV-induced ICAM-1 expression by Northern
blot analysis. RNA was isolated from control and RSV-infected A549
cells at the indicated times, purified, and separated on
glyoxal-agarose gels. RNA species were identified by Northern blot
analysis with 32P-labeled ICAM-1 probe. ICAM-1 mRNA is
detectable by 2 h, decreases by 6 h, and increases again at
all subsequent time points following RSV infection in A549 cells.
Results are representative of four experiments. C, control uninfected
cells; rsv, hours postinfection with RSV.
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FIG. 2.
RSV-induced ICAM-1 expression requires mRNA
transcription. The increased mRNA expression seen following RSV
infection requires increased gene transcription. ICAM-1 mRNA was
increased in RSV-infected cells but not in control cells. Following
actinomycin D treatment (10 µg/ml for 5 h) there was no
detectable ICAM-1 mRNA. Cycloheximide treatment alone (10 µg/ml for
5 h) had no significant effect on ICAM-1 mRNA concentrations.
Results are representative of three separate experiments.
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|
ICAM-1 promoter activity after RSV infection.
To confirm that
RSV-induced ICAM-1 upregulation occurred by activating gene
transcription, the ICAM-1 5'-flanking region was analyzed with
promoter/reporter gene constructs. The plasmid, pBH5000, which contains
5,000 bp of the 5'-proximal DNA fragment upstream to the ICAM-1
transcription start site, directing expression of the firefly
luciferase reporter gene, was obtained (Christian Stratowa and Dwight
Look [26, 30]) and transfected into A549 monolayers
(6, 7). Lysates from these cells demonstrated greatly
increased luciferase activity after RSV infection at all time points
(the greatest luciferase activity was 6 h following virus
exposure). Lysates from uninfected control cells demonstrated low
levels of luciferase activity comparable to those of cells transfected
with empty (promoterless) vector at all time points (Fig.
3). The time of peak activity differed
between the Northern analysis and the reporter studies, most likely
because of the difference between the time required for transcription,
translation, and posttranslational modification of the reporter
(luciferase) and the time required for transcription alone with
Northern analysis. This accounts for the decreased levels of ICAM-1
mRNA when the activity of the reporter is increased. Also, the
activities of both control (-galactosidase [-Gal]) and
ICAM-1-luciferase constructs were markedly decreased by 24 h
postinfection (48 h posttransfection) with this transient transfection
model, making it difficult to perform analyses at later time points due
to loss of plasmid or plasmid activity over time.
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FIG. 3.
The 5'-flanking region of the ICAM-1 gene confers RSV
responsiveness in A549 cells. A549 cells were transfected with pBH5000
and infected with RSV (multiplicity of infection, 1) for the indicated
times, and then cell lysates were harvested for measurement of
luciferase and -Gal activities. ICAM-1 gene activation (measured as
luciferase reporter gene activity) is significantly increased in A549
cells transfected with pBH5000 at all time points after RSV infection.
However, luciferase activity is greatest at the 6-h time point,
compared to the 2-h and 24-h time points. Results are the average of
six replicate samples. Luciferase activity is normalized to the -Gal
activity of that sample in order to correct for transfection
efficiency. Results are representative of two separate experiments.
Error bars represent standard deviations. **, P is
<0.01 compared to uninfected controls;  , P is <0.01
compared to 6-h RSV-infected cells.
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Functional significance of the ICAM-1 NF-B site after RSV
infection.
Initial studies were focused on the NF-B consensus
sequence in the ICAM-1 promoter (position 228). Monolayers of A549
cells were transfected with reporter constructs containing the normal or mutated NF-B sites (prepared by PCR with primers with normal or
mutated sequences) (6, 7) (Fig.
4A). Cells transfected with the construct
containing the normal NF-B site had greatly enhanced luciferase
activity after RSV infection (Fig. 4B). In contrast, the activation of
the luciferase gene following RSV infection was significantly decreased
in transfectants receiving mutated NF-B promoter constructs (Fig.
4B), comparable to that in uninfected control cells and cells
transfected with an empty vector (not shown).
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FIG. 4.
Mutational analysis of the ICAM-1 promoter region: the
roles of C/EBP and NF-B in RSV-induced ICAM-1 activation. (A)
Structure of NF-B and C/EBP reporter plasmids used in promoter
studies. This figure represents the cloning of the NF-B and C/EBP
reporter constructs used in the transfection studies. All constructs
were cloned into the KpnI and SalI sites of the
reporter plasmid pGL2-Basic. Capital letters in the bars indicate the
sequence of the normal transcription factor consensus sequence;
lowercase letters represent specific mutations introduced. The scheme
is not drawn to scale. All cell lysates for experiments that follow
were obtained 6 h following RSV infection. (B) Mutation of the
NF-B site at 228 eliminates RSV-induced ICAM-1 promoter activity.
A549 cells were cotransfected with pGL2-Basic containing the
appropriate NF-B consensus sequence and a second plasmid containing
the -Gal reporter gene. Twenty-four hours following transfection,
RSV was added to the cell monolayers and cell lysates were harvested
for measurement of luciferase and -Gal activities. RSV increased
luciferase activity of A549 cells transfected with the plasmid reporter
construct containing a normal NF-B site. This increase in luciferase
activity was eliminated in A549 cells transfected with the plasmid
reporter construct containing a mutated NF-B site. Results are the
average of six individual samples, with each sample corrected for
transfection efficiency relative to -Gal activity, and are
representative of three separate experiments. Error bars represent
standard deviations. Samples were obtained 6 h following RSV
exposure. *, P is <0.005 relative to control cells; ,
P is <0.005 relative to normal NF-B site. (C) Mutation
of C/EBP site at 239 decreases RSV-induced ICAM-1 promoter activity.
A549 cells were transfected with reporter plasmid constructs containing
the normal or mutated C/EBP consensus sequences and infected with RSV
as described above. ICAM-1 activation (measured as luciferase activity)
was significantly increased in A549 cells transfected with the plasmid
reporter construct containing a normal C/EBP site. This effect was lost
when cells were transfected with reporter constructs containing a
mutated C/EBP site. Results are the average of 4 to 6 samples, with
each sample corrected for transfection efficiency relative to
-Gal activity, and are representative of three separate experiments.
Error bars represent standard deviations. Samples were obtained 6 h following RSV exposure. **, P is <0.01 relative to
controls (either uninfected cells or cells transfected with
promotorless vector);  , P is <0.01 relative to
RSV-infected cells transfected with the normal C/EBP consensus
sequence.
|
|
Functional significance of the ICAM-1 C/EBP site after RSV
infection.
The C/EBP site adjacent to the NF-B site (239 bp)
was also examined. A549 cell monolayers transfected with pGL2-Basic
luciferase reporter constructs containing normal and mutated C/EBP
sites (prepared by PCR with primers containing normal or mutated C/EBP sequences) were infected with RSV 24 h later. Mutation of the C/EBP binding sequences significantly decreased promoter activation following RSV infection (Fig. 4A and C).
Comparison of RSV-induced and cytokine-induced ICAM-1
activation.
TNF-- and IFN--induced activation of ICAM-1 have
been reported to require different transcription factors. To compare
the mechanisms of transcriptional activation following RSV infection with TNF- and IFN- treatments, cells transfected with the
promoter constructs described above were incubated in the presence of
cytokine or infected with RSV, and cell lysates were prepared and
assayed for luciferase activity. Mutation of either the NF-B (Fig.
5A) or C/EBP sites (Fig. 5B)
significantly decreased ICAM-1 promoter activation following either
TNF- or RSV treatment. In contrast, mutation of either of these
sites had no effect on IFN--induced ICAM-1 activation. Ledebur et
al. demonstrated that TNF--induced activation of the ICAM-1 promoter
required the NF-B site targeted in the current studies
(13). In contrast, Look and coworkers (15, 16)
demonstrated that the IFN- response element located at nucleotides
130 to 194 of the ICAM-1 5'-flanking region conferred IFN-
responsiveness. The data presented here are consistent with the results
of these previous studies indicating that the NF-B and C/EBP binding
sequences in the ICAM-1 promoter are required for both TNF--induced
and RSV-induced ICAM-1 upregulation, whereas the IFN- response
element was unaffected by these mutations (Fig. 5).
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FIG. 5.
Mutational analysis of the ICAM-1 promoter region: roles
of C/EBP and NF-B in cytokine-induced ICAM-1 activation. (A) A549
cells were cotransfected with pGL2-Basic containing the appropriate
NF-B consensus sequence and a second plasmid containing the -Gal
reporter gene. Twenty-four hours following transfection, cell
monolayers were infected with RSV (multiplicity of infection, 1) or
treated with TNF- (5 ng/ml) or IFN- (10 ng/ml) for 6 h prior
to harvest of cell lysates. ICAM-1 gene activation was measured as
luciferase activity of the reporter plasmids. RSV and TNF (known to
increase ICAM-1 gene expression via the NF-B site at 228)
treatments increased luciferase activity of A549 cells transfected with
the plasmid reporter construct containing a normal NF-B site. This
increase in luciferase activity was eliminated in A549 cells
transfected with the plasmid reporter construct containing a mutated
NF-B site. In contrast, IFN- activation of the ICAM-1 promoter
constructs was unaffected by mutation of the NF-B binding site. Cell
lysates were obtained for luciferase measurements of 6 h following
virus exposure or cytokine treatment. Results are the average of three
samples, with each sample corrected for transfection efficiency
relative to -Gal activity, and are representative of three separate
experiments. Error bars represent standard deviations. *,
P is <0.01 relative to normal NF-B consensus sequence.
NS, no significant differences between IFN- treatment of cells
transfected with normal and mutated NF-B consensus sequences. (B)
Plasmid reporter constructs containing a normal and mutated C/EBP site
remained responsive to IFN, but mutation of the C/EBP site reduced
responsiveness to TNF- or RSV treatment. A549 cells were transfected
with reporter plasmid constructs containing the normal or mutated C/EBP
consensus sequences and were then treated as described for panel A. ICAM-1 activation (measured as luciferase activity) was significantly
increased in A549 cells transfected with the plasmid reporter construct
containing a normal C/EBP site following infection with RSV or TNF-
treatment. This effect was lost when cells were transfected with
reporter constructs containing a mutated C/EBP site. In contrast,
responses to IFN- were unaltered by mutation of the C/EBP consensus
sequences. Cell lysates were obtained for luciferase measurements
6 h following virus exposure or cytokine treatment. Results are
the average of three samples, with each sample corrected for
transfection efficiency relative to -Gal activity, and are
representative of three separate experiments. Error bars represent
standard deviations. **, P is <0.01 relative to mutated
C/EBP consensus sequences. NS1, no significant differences
between IFN- treatment of cells transfected with normal and mutated
C/EBP consensus sequences.
|
|
Researchers in several laboratories have demonstrated that activation
of NF-
B and NF-IL-6 occurs following RSV infection
of A549
monolayers (
6,
8,
9,
12,
17). Electrophoretic
mobility shift
and antibody supershift assays demonstrated that
NF-
B and NF-IL-6
activated following RSV infection (
6,
9,
17). In addition,
mutational and deletional analysis of the
IL-8 promoter demonstrated
that NF-IL-6 and NF-
B binding sites
located at
94 and
50 bp were
essential for RSV-induced IL-8
production. This arrangement of
transcription factor binding sites
is similar to the arrangement of
C/EBP and NF-
B sites in the
ICAM-1 promoter (
26). RSV
infection of the airway epithelium,
therefore, utilizes similar
mechanisms to regulate the orchestrated
production of ICAM-1 and IL-8
(
3).
Infections with viruses such as RSV trigger acute exacerbations of
asthma (
2,
24). RSV-induced NF-
B activation and the
subsequent upregulation of ICAM-1 and chemokines could contribute
to
inflammatory cell recruitment (
14,
31) and airway
hyperreactivity
following viral infection. Because of its pivotal role
in inflammation,
NF-
B will be an obvious target for new types of
anti-inflammatory
treatments for bronchiolitis or virus-induced asthma.
Blocking
the activation of NF-
B may prevent the early events in the
inflammatory
cascade, decreasing RSV-induced inflammation and
subsequent lung
injury.
In summary, we have shown that RSV regulates ICAM-1 gene expression at
the transcriptional level, acting through the 5'-flanking
region of the
ICAM-1 gene. The transcription factors NF-
B (
228)
and C/EBP
(
239) are necessary for RSV-induced ICAM-1 upregulation,
indicating
one molecular mechanism of virus-induced airway inflammation.
| |
ACKNOWLEDGMENTS |
These studies were supported in part by K08 HL02505 (J.M.S.), K08
HL03451 (M.A.F.), and grants from the American Lung Association and the
Cystic Fibrosis Foundation.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Division of
Pulmonary Medicine, Children's Hospital Medical Center, 3333 Burnet
Ave. OSB5, Cincinnati, OH 45229-3039. Phone: (513) 636-6771. Fax: (513) 636-4615. E-mail: starj0{at}chmcc.org.
| |
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J Virol, February 1998, p. 1623-1626, Vol. 72, No. 2
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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