Cao L et al / Acta Pharmacol Sin 2003 Dec; 24 (12): 1316-1323
CAO Lei2,3, QIAN
Li-Ling2, ZHU You-Rong2, GUO
Chun-Bao2, GONG Xiao-Hui2, SUN
Bo2,4
2Laboratory of Respiratory and Intensive Care, Children's Hospital of Fudan University, Shanghai 200032; 3Department of Pediatrics, Hebei Provincial People's Hospital, Shijiazhuang, China
1 Project supported by the National Natural Science Foundation (No 30170989).
4 Correspondence to Prof SUN Bo.
KEY WORDS acute lung injury; alveolar macrophages; NF-kappa B; activator protein-1; nitric oxide; surface-active agents; glucocorticoids
ABSTRACT
AIM: To investigate whether acute lung injury (ALI) in ventilated piglets
with bacterial infection affects NF-
B
and AP-1 expression in alveolar macrophages (AM) and whether nitric oxide (NO),
surfactant (Surf), glucocorticoids (GC) affect NF-
B
and AP-1 activation in AM in vivo and in vitro. METHODS:
The animals were intraperitoneally injected Escherichia coli, which caused
ALI. Nuclear extracts of AM were analyzed by electrophoretic mobility shift
assay (EMSA) for the nuclear factor-kappa B (NF-
B)
and activation protein-1 (AP-1) expression. Detection of I
B-
protein was from cytoplasmic extract by Western blotting. Immunocytochemistry
staining was used for intracellular location of p65 subunits of NF-
B.
RESULTS: In ex vivo experiments, strikingly higher expression
of NF-
B and AP-1 by EMSA was found
6 h after bacterial injection in contrast to the Normal group. In the NO, SNO,
and GC groups, markedly attenuated NF-
B
and AP-1 activation was observed. The NF-
B
and AP-1 activation in Surf group showed lower levels of the expression. Immunoblotting
of AM cytoplasmic extract showed low expression of I
B-
protein in the Control and Surf groups. The stronger expression was observed
in the NO, GC, and SNO groups. AM of the Control and Surf groups showed intense
nuclear staining, with decreased nuclear staining in the NO, GC and SNO groups.
In in vitro experiment, it caused a significant increase in NF-
B
and AP-1 activity in AM 1 h after exposure to lipopolysaccharides (LPS). In
AM treated by LPS+SNP and LPS+GC, all showed decrease of DNA binding activity
of NF-
B and AP-1 compared to those
exposed to LPS+Surf. Immunoblotting of AM cytoplasmic extract showed that LPS
stimulation of AM resulted in the low expression of I
B-
protein, which was not observed in the presence of SNP and methylprednisolone.
However, the surfactant did not show such effect. LPS+Surf-exposed AM had intense
nuclear staining, whereas decreased nuclear staining in the LPS+NO and LPS+GC-treated
cultures was found, confirming a decrease in NF-
B
activity. CONCLUSION:Activation of NF-
B
was found in AM of ventilated piglets with bacterial ALI. NO and GS could prevent
NF-
B and AP-1 activation in
vivo and in vitro. Surfactant has limited effects on NF-
B
and AP-1 activity.
INTRODUCTION
Inflammatory reaction in bacterial infection-induced aute lung injury (ALI) is characterized by
accumulation of large amount of macrophages and
neutrophils in the lungs, causing increased production of
immunally responsive cytokines and proteases as inflammatory mediators in the
lungs[1], amplifying ventilator- and/or oxygen-associated acute and chronic
damage. As a major effector of the innate immune
system of the body, alveolar macrophages (AM) interact
with other cells in airways and alveoli immediately after
birth, resulting in generation of intracellular signaling
cascades, leading to various effects or functions that
make up the initial immune response in the lungs.
Interaction of AM and lipopolysaccharides (LPS) or
bacterial infection causes a sequential activation of multiple
signaling pathways and transcription factors in AM,
resulting in gene transcription[2,3], orchestrating
production of both pro- and anti-inflammatory mediators in
the lungs. Two well-defined transcription factors
influenced by inflammation are nuclear factor kappa B
(NF-
B) and activation protein-1 (AP-1), which
play a significant role in regulation of the production of
many inflammatory mediators.
NF-
B is an ubiquitous transcription factor
complex that directs transcription of many cytokines,
adhesion molecules, and proinflammatory cytokine genes
that promote corresponding mRNA translation and
production of TNF-
, IL-1, IL-6, IL-8, IL-10, to
name just a few of the genes with active
NF-
B sites[4,5]. AP-1 belongs to a family of bZIP transcription
factors, which is characterized by a basic domain
required for sequence-specific DNA binding activity and
a region containing heptad repeats of leucine and
hydrophobic residues required for dimerization to other
bZIP protein family members[6]. AP-1 transcription
factors play critical roles in regulating target genes involved
in adaptive responses to inflammation. It is speculated
that activation of the inflammatory cascade involves the
activation of both NF-
B and AP-1 in AM, which
in turn induces and amplifies the expression of the
cytokines such as TNF-
, IL-1, IL-6,
IL-8, etc.
Acute inflammatory injury in ventilated infant lungs with bacterial infection,
or other causes such as share force stretching and hyperoxia, may rely on activation
of NF-
B and AP-1. There are limited
evidence regarding the role of AM in these activation events[7],
and fewer studies evaluated efficacy of NO[8], Surf and GC[9]
on expression of NF-
B and AP-1
in AM from in vivo ALI models with or without exposure to Gram negative
bacterial toxin, or LPS. We hypothesized that activation of NF-
B
may be central and pivotal to the development of pulmonary inflammation, and
therefore investigated whether acute inflammatory injury in ventilated piglets
with bacterial infection affects NF-
B
and AP-1 activation in AM, and whether exogenous NO, Surf, and GC may alleviate
expression of NF-
B and AP-1 activation
in AM ex vivo and in vitro.
The lung exposed to risk factors such as meconium aspiration, hyperoxia, and infection frequently
develops ALI. These injuries, occurring in
developmentally and structurally immature lungs are thought to
contribute to the pathogenesis of chronic lung disease
(CLD). As a major effector of the innate immune
system of the body, AM interact with other cells in
airways and alveoli immediately after birth, resulting in
generation of intracellular signaling cascades, leading
to various effects or functions that make up the initial
immune response in the lungs and cause activation of
NF-
B and AP-1, resulting in gene transcription.
MATERIALS AND METHODS
Ex vivo experiments
Animal model Healthy piglets were obtained from a local farm (Institute of Veterinary Medicine, Shanghai Academy of Agricultural Science, Shanghai). The animals, 3-5 weeks old and weighing 7-11 kg, were anesthetized and intubated. Each piglet was ventilated with a Servo 900C ventilator (Siemens-Elema, Solna, Sweden). Intravasular catheters were placed for blood gas measurement and fluid infusion as required for standard care. The animals were randomly allocated to 6 groups (n=6 per group). A Normal group was not subjected to bacterial injection but identical ventilation and management. The other animals were intraperitoneally injected with 5 mL of Escherichia coli (E coli ATCC 25922, 1×1012-2×1012/L), which caused ALI after 2-6 h. ALI was evidenced in animals with intraperitoneal injection of Escherichia coli by marked decrease of paO2/FiO2 less then 300 mmHg, and dynamic lung compliance (Cdyn) values more than 30 % compared with baseline. A control group received no additional treatment, and the other piglets were assigned to one of the four treatment groups: NO, inhaled NO at 10 ppm[10]; Surf, a porcine surfactant preparation[11] at phospholipids of 100 mg/kg body weight in 2.5 mL, instilled intratracheally; SNO, a combined treatment of surfactant and inhaled NO as for NO and Surf groups; GC, iv methylprednisolone (Pharmacia & Upjohn, Puurs, Belgium) at 20 mg/kg. During the treatment, ventilator settings were regulated and standard care was given to maintain adequate gas exchange, blood pressure and electrolyte and fluid balance. The animal experiments were subjected to the other protocols also, hence the data regarding lung function in vivo, biochemistry and morphology are not reported herewith.
Airway aspiration procedure Three milliliters of normal saline was instilled in two 1.5-mL aliquots through a suction tubing introduced via a slide valve in the endotracheal tube connector until resistance was met. After the first aliquot administration the piglet was ventilated for a few minutes and a second aliquot was administered. Recovered fluid volume varied between 40 % and 80 % of the initial volume instilled, and two aliquots were combined in a sterile test tube and transported on ice to the laboratory for processing immedi-ately. Airway aspitate (AA) samples for all time points were taken from the same animal: immediately after intratracheal intubation, 2 h after bacterial administration, establishment of ALI, and 6 h of the treatment, respectively.
AA cell counts One sample of the recovered AA fluid was used for microbiological and cytological study including total and differential cell count (DCC) after cytocentrifuge preparation. Manual DCC were performed for each AA specimen following Wright staining, and 300 cells per cytospin were counted.
Alveolar macrophage isolation AM in AA fluid were isolated by differential adherence. Obtained AA cells were collected by centrifugation at 400×g for 10 min at 4 ºC, then washed once with Hanks' balanced salt solution. RPMI-1640 medium (Glutamax, Gibco Life Technologies, Paisley, UK) was supplemented with 20 % fetal bovin serum (FBS) and 50 U penicillin G and 50 µg streptomycin per mL of medium. The washed cells were suspended at a concentration of (3-5)×108 cells/L in RPMI-1640 medium, added to 35-mm dishes, and incubated at 37 ºC in 5 % CO2 to allow adherence of AM. After 2 h of incubation, the nonadherent cells were discarded, and the monolayer, containing more than 95 % AM, as determined by Wright staining, was washed with PBS. AM obtained from bacteria-infected lungs were used for ex vivo experiments, and those from the Normal lungs, for in vitro experiments,.
Preparation of nuclear and cytoplasmic protein fractions Preparation of nucleus was extracted according to manufacturer's instruction of NE-PERTM nuclear and cytoplasmic extraction reagents kit (Pierce, Rockford, IL) and the extracts were kept at -80 ºC for further use. The protein content of AM was determined with the bicinchoninic acid protein assay kit (BCA, Pierce).
Oligonucleotide labeling Oligonucleotides were labeled using a double-stranded
consensus sequence NF-
B (5'-AGTTGAGGGGACTTTCCCAGGC-3',
Pro-mega, Madison, WI) and AP-1 (5'-CGCTTGATGA-GTCAGCCGGAA-3', Promega) and
-32P]-ATP (Yahui, Beijing,
China). The reaction was catalyzed with T4 polynucleotide kinase
and incubated in 10×kinase buffer at 37 ºC for 45 min. The reacion
was stopped by heating at 65 ºC for 10 min. Purification of the labeled
oligonucleotides was performed with the QIAquick Nucleotide Removal kit (Qiagen,
Valencia, Spain) according to the manufacturer's instructions.
Electrophoretic mobility shifting assay Nuclear extracts was analyzed by EMSA[10]. Binding reactions containing equal amounts of nuclear protein extract (10 µg) and 35 fmol of oligonucleotide were performed for 30 min in binding buffer (Promega). Reaction volumes were held constant to 15 µL. For experiments of specific competitor, a 50-fold excess of unlabeled ("cold") oligonucleotide was used and for experiments of nonspecific competitor, SP-1 (Promega, O-glycosylated transcription factor) were used. For a supershift assay, each sample was incubated with anti-p65 antibody 1 µg (Santa Cruz Biotechnology, Santa Cruz, CA) for 30 min at room temperature before addition of the probe. To distinguish nonspecific binding of the AP-1, competition reactions were performed by adding 50-fold excess of nonradiolabeled AP-1 to the binding reaction mixture before electrophoresis. Reaction products were separated in a 4 % polyacrylamide gel in 0.5×TBE buffer (Tris base, boric acid and edetic acid) and analyzed by autoradiography. Autoradiograms were quantified using Imagequant analysis software (Shenteng, Shanghai, China).
Western blot for inhibitor of NF-
B
(I
B-
) protein Cytoplasmic
extract from cultured cells was prepared with the Pierce NE-PERTM
kit (Pierce) and kept at -80 ºC. The protein content of AM was determined
with BCA kit. Fifty micrograms of cytoplasmic protein extracts were separated
by 12 % sodium dodecyl sulfate acrylamide gel electrophoresis, and electrotrans-ferred
(40 mA, 2 h) onto a nitrocellulose membrane (Bio-Rad, Hercules, CA), The membranes
were blocked with 10 % FBS in PBS for 2 h. The membrane was washed three times in 1×PBS-0.05 %
Tween 20 and subsequently incubated with a rabbit polyclonal
anti-I
B-
antibody (SC371,
0.5 mg/L; Santa Cruz, Santa Cruz, CA) for 1 h. The
membrane was washed three times in 1×PBS-0.05
%-Tween 20 and incubated with goat anti-rabbit
horseradish peroxidase-conjugated secondary antibody for 1
h. After successive washes, the membrane was
developed with an enhanced chemiluminescence kit (SuperSignal Western Blotting kit, 34094, Pierce)
according to manufacturer's instructions. Quantification
of I
B-
levels was done with
densitometer and Imagequant software (Shenteng, Shanghai,
China).
Immunocytochemical staining for intracellular location of p65 AM were cultured on coverslips and the cells were fixed after 4 h, and stained with anti-p65 antibody. AM were plated (1×106 cells per well) in each well of 6-well plates containing glass coverslips, and allowed to adhere for 2 h, The coverslips were rinsed with PBS, and the adherent cells were fixed for 2 min in cold 4 % paraformaldehyde, and stored at -20 ºC until stained. Before staining, the coverslips were rinsed in PBS (pH 7.4) for 10 min, and then blocked with 2 % goat serum for 15 min, briefly rinsed in PBS, and stained with anti-p65 antibody (Santa Cruz) for 60 min in a humid chamber. Following this, coverslips were washed thrice in PBS and biotinylated secondary antibody in 2 % goat serum was added, then the coverslips were incubated in a humid chamber for 1 h. The coverslips were incubated in peroxidase substrate for 5 min and then washed thrice in PBS, mounted on slides and sealed with clear nail polish.
In vitro experiments AM obtained from AA of normal piglets during
early stage of mechanical ventilation were first centrifuged at 500×g at
4 ºC. The cell pellet was immediately maintained in RPMI-1640 medium with
FBS and antibiotics and allowed to adhere for 2 h at 37 ºC and 5 % CO2
incubator. For in vitro experiments, AM were allowed to adhere and rest
by indicated treatments. The best time of treatments and the best concentration
of drugs were determined by pre-experiments. LPS (from Escherichia coli,
Sigma, Lot 85H4092) was used at 1 µg/L 1 h for all experiments. Then the
cells were either treated with sodium nitro-prusside (SNP, NO donor) at 100
µg/L, or with Surf at 2 g/L, or with methylprednisolone at 0.3 µg/L.
Nuclear extracts were then prepared after 2 h incubation as described in preparation
of nuclear extracts and EMSA. Quantification of I
B-
was performed as above described in preparation of cytoplasmic extracts
and detection of I
B-
protein by the Western blotting. Immunocytochemical staining for intracellular
location of p65 were also performed as described above.
Statistical analysis All the values are expressed as means±SD of at least five separate experiments in both ex vivo and in vitro experiments. Between-groups differences of the data from ex vivo and in vitro experiments were subjected to a one-way analysis of variance (ANOVA), and between-group differences were further compared with Student-Newman-Keuls post hoc test. Significance of the differences was defined as P<0.05.
RESULTS
Ex vivo experiments
NF-
B and AP-1 activation in
AM from ventilated piglets No clear effect of enhanced expression of NF-
B
and AP-1 activation was seen in all groups at early time of intratracheal intubation
and 2 h after bacterial injection. However, strikingly higher expression of
NF-
B and AP-1 by EMSA was found
6 h after bacterial injection (ALI was established) as reflected by substantially
enhanced binding complexes of NF-
B
and AP-1 from the nuclear extracts of AM in contrast to the same group 2 h after
bacterial injection and the Normal group (without bacterial injection). In the
NO and GC groups, markedly attenuated NF-
B
and AP-1 activation was observed compared to the control group at 6 h. The NF-
B
and AP-1 activation in Surf group showed moderately lower levels of the expression,
but in the SNO group attenuated NF-
B
and AP-1 activation remained obvious, compared to the control at 6 h after the
treatment (Fig 1A-C).
Fig 1. NF-
B and AP-1 activity in nuclear extracts of alveolar macrophages
(AM). A: EMSA for NF-
B activity in nuclear extracts of AM ex vivo. Lane
1, normal (N); 2, control (C); 3, nitric oxide (NO); 4, glycocoticoids (GC);
5, surfactant (Surf); 6, Surf and NO (SNO); 7, nonspecific competitor;
8, specific competitor. B, C, D and E: Densitometric analysis for EMSA bands
of nuclear extracts of AM by image analysis system. n=6. Mean±SD.
B and C for NF-
B and AP-1 activity in AM ex vivo, respectively.
cP<0.01 vs Control; D and E for NF-
B and AP-1 activity
in AM in vitro, respectively. cP<0.01 vs
LPS.
I
B-
protein expression
Immunoblotting of AM cytoplasmic extract with an anti-I
B-
antibody showed low expression of I
B-
protein in the Control and Surf groups. The stronger expression was observed
in the NO, GC, and SNO groups (Fig 2A-B).
Fig 2. I
B-
levels in cytoplasmic extracts of AM. A: Western blotting for
I
B-
levels in cytoplasmic extracts of AM. Lane 1, Normal (N); 2, GC; 3, NO;
4, Surf; 5, SNO; 6, Control (C). B and C: Densitometric analysis for Western
blotting bands of cytoplasmic extracts of AM by image analysis system. n=6.
Mean±SD. (B) for I
B-
levels in AM ex vivo. cP<0.01
vs Control); (C) for I
B-
levels in AM in vitro.
cP<0.01 vs LPS.
Immunocytochemical staining for intracellular location of p65 Minimal nuclear
staining for p65 in the cytoplasm of AM in the Normal group was seen. AM of
the control and Surf groups showed intense nuclear staining, with decreased
nuclear staining in the NO, GC, and SNO groups, confirming a decrease in NF-
B
activation. Despite the translocation of NF-
B
to the nucleus, the cytoplasm remained with yellow light as a large portion
of the NF-
B complex was retained
in it (Fig 3).
Fig 3. Immunocytochemical staining for intracellular location of p65. A:
normal group, AM were not activated and the p65 (NF-
B) staining remained localized
to the cytoplasm. B: control group, AM were activated and the NF-
B migrated
to the nucleus and nuclei appear yellow. C: NO group, nuclear staining with
p65 was decreased in AM compared with the control group.
In vitro experiment
NF-
B and AP-1 activation of
LPS-stimulated AM One hour after exposure to LPS, it caused a significant
increase in NF-
B and AP-1 activity
in AM. In AM treated by LPS+SNP and LPS+GC, all showed decrease of DNA binding
activity of NF-
B and AP-1. No
increased NF-
B and AP-1 activity
was observed in AM exposed to LPS+Surf compared to those exposed to LPS only
(Fig 1D-E).
Immunoblotting of I
B-
protein
Immunoblot-ting of AM cytoplasmic extract with the anti-I
B-
antibody showed that LPS stimulation of AM resulted in the low expression of
I
B-
protein, which was not observed in the presence of SNP and methylpredniso-lone.
However, the surfactant did not show such effect (Fig 2C).
Immunocytochemical staining for intracellular location of p65 LPS+Surf-exposed
AM had intense nuclear staining, whereas decreased nuclear staining in the LPS+NO
and LPS+GC-treated cultures was found, confirming a decrease in NF-
B
activation.
DISCUSSION
AM is an important source of cytokines and growth factors in the lungs[5],
and many cytokines are regulated by the redox-sensitive transcription factor,
NF-
B[4]. NF-
B
consists of a heterodimer of p50 and p65 subunits, which are retained in most
cells in the cytoplasm in complex with inhibitory proteins of the inhibitor-
B
family. In unstimulated cells, NF-
B
resides in the cytoplasm as a dimer of protein components known as Rel family
member (eg, p50, p65[12], which is bound to an I
B.
Upon stimulation or activation, I
B
is phosphorylated and released from the complex, after which the complex undergoes
proteolytic degradation and the Rel proteins migrate to the nucleus and bind
to the cognate sites in the promoter regions of the genes for many inflammatory
cytokine and growth factors[5], resulting in their transcription[12].
Increasing evidence suggests an important role for NF-
B
in the pathogenesis of lung inflammation. Results from the study have shown
that NF-
B regulates gene expression
of cytokines[4]. These in vitro findings are supported by
studies in humans with ARDS that enhanced NF-
B
activation was found in AM recovered by AA[13]. Some recent in
vivo studies have demonstrated that lung NF-
B
activation is suppressed by NO[8] and GC[9], resulting
in decreased proinflammatory mediator expression and reduced inflammatory injury[14].
Thus, it appears that activation of NF-
B
may be central and pivotal to the development of pulmonary inflammation.
The transcription factor AP-1 is a known stress response complex that functions in signal transduction by inducing the expression of specific downstream genes[15]. The AP-1 complex consists of various heterodimers of fos/jun proteins or homodimers of jun/ jun proteins. Several mechanisms are believed to be involved in regulating AP-1 transcriptional activity, including differential gene expression of fos or jun, conformational alterations, posttranslation modification, and altered DNA- binding specificities of the heterodimers. AP-1 DNA-binding activity can be modulated by a direct association between thioredoxin and Ref-1[16]. There is little direct evidence regarding the role of AM in these activation events. We observed that AM from piglets had enhanced AP-1 binding activity after bacterial exposure in vivo and LPS exposure in vitro. The underlying mechanism of this alteration requires further investigation to correlate it with severity of the inflammation and injury.
We also investigated whether NO, Surf and GC affected
NF-
B and AP-1 activation in
vitro. In AM from the Normal animal lungs and stimulated by
LPS subsequently in vitro, we compared their response
in the absence and presence of NO, Surf, and GC (methyl-prednisolone), and found that NO and GC
suppressed NF-
B and AP-1 activity in similar
magnitude, but the Surf had apparently less effect on it.
NO is an inorganic free radical and a remarkably
versatile biological messenger. The chemical properties of
NO are crucial in defining its biological roles as both a
transcellular signal in the cardiovascular and nervous
systems and a cytotoxic antipathogenic agent released
during inflammatory response. NO is an important
endogenous regulatory molecule synthesized in various
cells of the lungs, and involved in many diverse
physiologic processes[17,18]. However, there is scarce
information about NO metabolite affecting the activating
process of NF-
B and AP-1. It has been shown
that NO donor agents suppress NF-
B
activation in human endothelial cells in
vitro by increasing the level of
I
B[19]. In contrast, studies with human
peripheral blood lymphocytes have demonstrated
activation of NF-
B in the presence of NO
donors[20]. Currently, there is no explanation for these
conflicting results. Subtle differences in experimental
design, cell type specialty, difference of NO donors,
and prestimulation of cells may account for the
different results. Our ex vivo findings indicate that NO is
anti-inflammatory through decreasing
NF-
B and AP-1 activation and therefore has a potential role in
protection of the lungs from ALI.
Understanding NO function may lead to ways of modulating inflammatory response. SNP is often used
as an NO donor for clinical and laboratory experiment.
The vasodilator effects of SNP are believed to be largely
mediated by NO, but its mechanism of action remains
uncertain[21]. In the present study, we found that NO
decreased NF-
B and AP-1 in AM in
vitro. I
B-
protein levels were greater in
cytoplasmic extraction from LPS+SNP-treated than in those
from LPS-treated cells. These results indicate that NO
prevented NF-
B activation by maintaining a
steady-state level of I
B-
protein, an
effect that may be mediated by increase of
I
B synthesis and/or decrease of
I
B degradation.
Despite wide use of GC in clinical disorders, the
mechanism of anti-inflammatory action of GC is not
completely defined. GC effects are mediated through
an intracellular receptor, the GC receptor, a member of
the steroid hormone receptor
superfamily[22]. Upon hormone binding, the cytoplasmic GC receptor can enter
into nucleus, dimerize, and bind to specific DNA
sequences located in the 5' promoter region of many genes,
leading to modulation of gene
transcription[23]. The activated GC receptor may also interact with other
transcription factors such as NF-
B and AP-1, to
regulate gene transcription[24]. In
vitro studies have shown that some of the anti-inflammatory actions of
GC are due to inhibition of
NF-
B[25,26]. Although GC are useful in the treatment of some inflammatory
diseases, their role for mitigation of severity of
pulmonary inflammatory injury in mechanical ventilation with
bacterial infection remains uncertain. Because
previous studies with GC in animal models of lung injury
have shown variable results[27], our results indicate that
the actions of GC on inflammatory process are complex and certainly involve
NF-
B and AP-1.
Surfactant treatment is a standard care for premature newborn infants with respiratory distress
syndrome due to surfactant deficiency and lung immaturity.
Surfactant suppresses streptococcal proliferation in
neonatal pneumonia, and also has a potential to inhibit
proinflammatory cytokine release from AM or mononuclear
leukocytes[28]. The recent study has shown that
SP-A dramatically inhibits activation of
NF-
B in AM stimulated with
LPS[28]. Another study showed that phospholipids of surfactant can downregulate the
immune response[29]. In the in
vitro experiments, release of inflammatory cytokines by human AM was inhibited
by lipid components of the
surfactant[30]. Thus, the surfactant lipids may have anti-inflammatory actions in
the alveolar space. Nevertheless, the exact mechanisms
are incompletely understood. We found that in the
ex vivo study, surfactant (phospholipids
with SP-B and SP-C, no SP-A) had variable effects on
NF-
B and AP-1 activation in piglet AM, but it had no effects
in inhibition of activation of NF-
B and AP-1 in
AM stimulated with LPS in vitro. Our results suggest
that the anti-inflammatory effects of the surfactant
lipids may not be exerted through NF-
B and AP-1
signaling pathways, and is consistent with another
author[31].
AM activation is an initial event in the genesis of
lung inflammatory reactions. Furthermore,
NF-
B activation in AM in vivo occurs prior to
NF-
B activation in whole-lung tissues, suggesting that
products of activated AM are required to stimulate
nuclear translocation of NF-
B in other lung-cell
types[32]. The present data support that
NF-
B activation is pivotal in the pathogenesis of lung
inflammation. In our in vivo experiments by examining
freshly isolated AM from normal piglets and ventilated
piglets with bacterial infection, we have established a
method to obtain in vivo "silent" or inflammation
activated AM as characterized by their response to
in vitro stimulations leading to up- or down-regulation of
expression of NF-
B intracellularly. This enables
further study in the mechanism of interaction between
inflammatory cells and lung cells in ALI, and growth
factor-mediated lung cell proliferation and reparation.
We conclude that interaction of LPS or bacterial
infection with AM causes a sequential activation of
NF-
B and AP-1 signaling pathways, resulting in gene
transcription. Activation of NF-
B and AP-1 in
AM of ventilated piglets with bacterial infection may be
downregulated by NO and GC. Surfactant has limited
effects in regulation of NF-
B and AP-1 activity.
Further studies are required to elucidate the role of
NF-
B in mediating signal transduction in pulmonary
cell proliferation and reparation in septic ALI, and its
modulation in preventing biotrauma as seen in ARDS.
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