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Laboratoire de Chirurgie Expérimentale, Jeune Equipe 324, Centre Chirurgical Marie Lannelongue, Université de Paris Sud, Le Plessis Robinson 92350; and Laboratoire de Chimie Organique et Multifonctionelle, Université de Paris Sud, Orsay 91405, France
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Reignier, Jean, Hassan Sellak, Rémy Lemoine,
André Lubineau, Guy Michel Mazmanian, Hélène Detruit,
Alain Chapelier, Philippe Hervé, and The Paris-Sud University
Lung Transplantation Group. Prevention of ischemia-reperfusion
lung injury by sulfated Lewisa
pentasaccharide. J. Appl. Physiol.
82(4): 1058-1063, 1997.
Inhibition of polymorphonuclear
neutrophil (PMN) adhesion to the pulmonary endothelium attenuates
ischemia-reperfusion (I/R) lung injury. We hypothesized that
3
-sulfated Lewisa (SuLa), a
potent ligand for the selectin adhesion molecules, may have a
beneficial effect on I/R lung injury, as measured by the filtration
coefficient
(Kfc),
and reduce pulmonary sequestration of PMN as assessed by the lung
myeloperoxidase (MPO) activity. Blood-perfused rat lungs were subjected
to 30 min of perfusion, 60 min of warm ischemia, and 90 min of
reperfusion after treatment with either SuLa (200 µg) or saline.
Effects of SuLa on PMN adhesion to cultured human umbilical vein
endothelial cells (HUVEC) stimulated with tumor necrosis factor-
and
calcium ionophore were also investigated. Compared with preischemia
conditions, I/R induced a significant increase in
Kfc,
which was attenuated with SuLa (80 ± 8 vs. 30 ± 5%; P < 0.001). SuLa reduced lung
MPO and PMN adhesion to stimulated HUVEC. These results indicate that
SuLa reduces I/R-induced lung injury and PMN accumulation in lung. This
protective effect might be related to inhibition of PMN adhesion to
endothelial cells.
endothelium; selectins; neutrophils; rat lung
INTRODUCTION ISCHEMIA-REPERFUSION (I/R) lung injury occurs after
lung transplantation, pulmonary thromboendarteriectomy, or
cardiopulmonary bypass. Increased microvascular permeability and
polymorphonuclear neutrophils (PMN) lung sequestration are
well-described consequences of lung I/R. The reperfusion of ischemic
lungs initiates an inflammatory cascade characterized by the
elaboration of cytokines and proinflammatory mediators, such as
platelet-activating factor and leukotriene B4 (10, 12, 27), the expression of
cell adhesion molecules (6, 7, 13), the adhesion of PMN to the
pulmonary endothelium (2, 19), and finally PMN-mediated lung injury (1,
3, 13). Studies aimed at the removal or inhibition of PMN have demonstrated a dramatic reduction in I/R lung injury and provide evidence that PMN play a major role in lung reperfusion injury (6, 21,
22).
The initial interaction between PMN and endothelial cells is mediated
by the selectin adhesion molecules (9, 10, 29). The selectins initiate
rolling and tethering of PMN to the endothelial surface and facilitate
exposure to various PMN activators. This rolling is the first step in a
sequence of events leading to firm adhesion of activated PMN to the
endothelium, which is induced by PMN
Recent studies indicate that administration of monoclonal antibodies
directed against P-selectin (8, 31) or both L- and E-selectins improves
lung reperfusion injury (26). Soluble carbohydrate ligands to selectins
may also have the potential to attenuate I/R-induced PMN-endothelial
interactions (11). Indeed, each selectin shares a common molecular
structure, most notably an NH2-terminal lectin-like domain,
which suggests that the selectins might bind to oligosaccharides on
other cells. To date, three structures have been identified that appear
to have binding affinity for selectins:
1) oligosaccharides
related to sialyl Lewisa and
sialyl Lewisx,
2) phosphorylated
mono- and polysaccharides, and
3) sulfated polysaccharides and lipids (17, 18, 29). The discovery that selectin-mediated adhesion is dependent on carbohydrate
binding has generated a great deal of interest in creating bioactive
and biostable analogs of Lewisx
and Lewisa. Sialyl
Lewisx tri- and tetrasaccharides
were recently shown to attenuate PMN accumulation and lung injury in
rats subjected to acute lung inflammation mediated by either P- (18) or
E-selectin (17). A sialyl Lewisx
analog was also shown to attenuate PMN accumulation and myocardial necrosis in a canine model of myocardial I/R (11). Recent in vitro
studies demonstrate that the 3 Accordingly, we reasoned that SuLa might be able to attenuate the lung
reperfusion insult and reduce PMN lung sequestration by decreasing PMN
adhesion to endothelial cells. To test this hypothesis, we subjected
isolated blood-perfused rat lungs to ischemia followed by reperfusion
in the presence or in the absence of SuLa. More specifically, the
objectives of the present study were
1) to investigate
the ability of SuLa to reduce the I/R-induced increase in microvascular
permeability, 2) to
assess the effect of SuLa on the pulmonary sequestration of PMN during
reperfusion, and 3)
to investigate whether SuLa might inhibit PMN adhesion to endothelial
cells in vitro.
METHODS Isolated Perfused Rat Lung
2-integrin (CD11/CD18) and its
endothelial ligands, intercellular adhesion molecule-1 or -2 (ICAM-1 or
ICAM-2) (6, 7). After adhesion to the pulmonary endothelium, PMN can
undergo activation and release numerous toxic substances including
oxygen-derived free radicals, inflammatory cytokines,
platelet-activating factor, leukotriene
B4, elastase, myeloperoxidase
(MPO), and other proteolytic enzymes (2).
-sulfated
Lewisa (SuLa) pentasaccharide is a
more potent ligand to E- and L-selectins compared with sialyl
Lewisx analogs (5, 30).
1 · min1.
Pulmonary effluent blood was collected into a plastic reservoir through
the cannula placed in the left atrium. Pulmonary arterial pressure
(Ppa) and pulmonary venous pressure (Ppv) were continuously monitored
with P23 ID transducers (Statham) connected to an amplifier (model M52;
Telco). A cannulating probe (model 1517-025; Statham) connected to
an electromagnetic flowmeter (model 2201; Statham) was placed in series
with the perfusing circuit for continuous pulmonary blood flow
(
) monitoring. and pressure
signals were recorded on a multichannel chart recorder (Alco ED 69).
Zone 3 conditions (arterial > venous > alveolar pressures) were
maintained throughout all experiments.
Pulmonary Capillary Pressure (Ppc)
Ppc was estimated by using the double occlusion method (28). Arterial inflow and venous outflow were occluded simultaneously, causing Ppa and Ppv to equilibrate at a pressure well correlated with Ppc. Pulmonary arterial and venous resistances (Ra and Rv, respectively) were calculated as follows
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Kfc
Kfc was used as the index of endothelial permeability to fluid. Kfc was measured by using the isogravimetric method described by Drake et al. (4). After an isogravimetric period of 30 min, Ppv was rapidly increased by 8 cmH2O for 15 min by raising the outflow end of the left atrium cannula. The increase in lung weight was recorded. A characteristic rapid weight gain due to vascular filling was followed by a slower rate of weight gain reflecting filtration of fluid into the pulmonary interstitium. The rate of slow weight change (
Wt/t) was
analyzed by using linear regression of the
log10-transformed weight
changes/min. The initial rate of weight gain was calculated by
extrapolating Wt/t to
time 0.
Kfc
was calculated by dividing Wt/t
at time
0 by the change in Ppc
that occurred after venous outflow pressure was increased, normalized
for the baseline wet lung weight and expressed as
ml · min1 · cmH2O1 · 100 g lung tissue1.
MPO Activity
The method described by Mullane (16) was used to measure MPO activity in the lungs. The lungs were frozen in liquid N2, pulverized, and then homogenized in 10% wt/vol of hexadecyltrimethyl ammonium bromide (HTAB) buffer (0.5% HTAB in 50 mM phosphate buffer, pH 6.0) with a Polytron homogenizer. The homogenate was sonicated on ice for 15 s, frozen at
70°C, thawed three times, then centrifuged at
40,000 g for 15 min.
The supernatant was assayed for MPO activity spectrophotometrically.
Then 20 µl of supernatant were combined with 12 µl of 25 mM
H2O2,
30 µl of 40 mM O-dianisidine
hydrochloride, and 1.938 ml of 50 mM phosphate buffer (pH 6.0). The
change in absorbance was measured at 460 nm on a Beckman spectrometer
(model 25; Beckman, Fullerton, CA). One unit of MPO activity is defined as the activity degrading 1 µmol of
H2O2/min
at 25°C.
Synthesis of the SuLa Pentasaccharide
The Lewisa pentasaccharide was sulfated at position 3 of the outer galactose (14). It was prepared by using the 4-methoxybenzyl glycoside of N-acetylglucosamine as starting material. The synthesis of the pentasaccharide was achieved through a-stereoselective coupling of an -trichloroacetimidate-activated
form of the N-acetamido-protected trisaccharide onto a 3, 4-unprotected lactose derivative
(14).
In Vitro Adhesion of PMN to Human Umbilical Vein Endothelial Cells
Human umbilical vein cords were treated with 0.05% collagenase, and human umbilical vein endothelial cells (HUVEC) were harvested as described elsewhere (25). Cells were suspended in the culture medium (M199 containing 20% heat-inactivated bovine calf serum, L-glutamine, fungizone, penicillin-streptomycin) and initially seeded in gelatin-coated 35-mm dishes. Nonadherent cells were removed after 2 h. Confluent endothelial cells were passed after treatment with trypsin-EDTA (0.05-0.02%, respectively). Inverted microscopy was used to assess endothelial cell purity shown by a typical "cobblestone" appearance. All experiments were performed with the use of endothelial cells at second passage seeded in 24-well gelatin-coated culture plates.PMN were recovered from heparinized blood of healthy donors and then purified as described elsewhere (25), by a process including sedimentation on 2% Dextran T-500 and centrifugation on a Ficoll-Paque density gradient, followed by hypotonic lysis of residual erythrocytes. The preparation contained >95% PMN, and viability as assessed by trypan blue exclusion was >97%.
HUVEC were stimulated with tumor necrosis factor- (TNF-) or
calcium ionophore (CaI) for 4 h and 15 min, respectively. SuLa (100 µmol/l; n = 4) or saline
(n = 4) were then added to stimulated HUVEC during 15 min at 4°C. PMN
(106/ml) were added to washed
HUVEC. After 30 min of contact, unbound PMN were removed by three
washes with buffer. Adherent PMN were collected, lysed (1% Triton
X-100), and sonicated three times at 10 s each. MPO in the adherent PMN
fraction was measured as previously described (25). Adherence was
expressed as the percentage ratio of the MPO measured in adherent PMN
to the MPO measured in the PMN
(106/ml) added initially.
Specific Protocols
After being placed in the temperature-controlled, humidified chamber, the lungs were allowed to equilibrate for 30 min and were made isogravimetric by adjusting Ppv. Then, after determination of the baseline values (Ppa, Ppv, Ppc, and Kfc), one of the following protocols was followed. Time-control lungs (n = 6). After the baseline determinations, the lungs were subjected to 3 h of perfusion. Ppa, Ppv, Ppc, and Kfc were again determined at the end of this period. I/R lungs (n = 12). After the baseline determinations, ventilation and perfusion were interrupted, and the lungs were maintained in the humidified chamber at a temperature of 37°C for 60 min. After the arterial and venous cannulas were clamped, the recirculating blood was discarded, and the external circuit was flushed with saline. After this period of ischemia, the lungs were randomly allocated in two groups: 1) I/R control (n = 6; treated with saline), and 2) I/R SuLa (n = 6; treated with 200 µg of SuLa). New fresh blood was obtained from two donor rats, and saline or SuLa was then added. Hematocrit was adjusted to 28% at the beginning of each period (i.e., baseline and reperfusion) by addition of saline. After a 90-min isogravimetric period of reperfusion, measurements of Ppa, Ppv, Ppc, and Kfc were performed. Before and after the reperfusion period, platelets and white blood cell (WBC) counts (n = 6 in each group) were performed in the venous effluent to allow determination of the percentage decrease in circulating PMN count during reperfusion. At the end of experiment, the lungs were flushed with saline at a low flow of 5 ml/min during 5 min, and lungs were frozen for determination of MPO activity (n = 6 in each group).Reagents
M199 culture medium, fetal bovine serum, L-glutamine (200 mM), penicillin-streptomycin (5,000 UI/ml-5,000 µg/ml), fungizone (250 µg/ml), trypsin-EDTA (0.5-0.2 g/l), and Hank's balanced salt solution were from GIBCO (Cergy-Pontoise, France). TNF-
was from Promo Cell (Heidelberg, Germany). Triton X-100, CaI, and
orthodianisidine were from Sigma (St. Louis, MO). The 24-well
gelatin-coated culture plates were obtained from Corning Glass
(Corning, NY). Dextran T-500 and Ficoll-Paque were from Pharmacia
Biotech (Upsala, Sweden). Collagenase (Collostrum
histidicum) was from
Boehringer (Mannheim, Germany).
Statistics
All results are expressed as means ± SE. Baseline and final measurements of Kfc and hemodynamic variables of different groups were compared using a two-way analysis of variance for repeated measurements. Newman-Keuls test was used as a post hoc test. Lung MPO activity and adherence were compared by using an independent Student's t-test. Significance was determined when P < 0.05 was obtained.RESULTS
Baseline values of Ppa, Ppv, Ppc, Rpa, Rpv, and Kfc were similar in the three groups.
Kfc
values are shown in Fig. 1. After 3-h
perfusion,
Kfc
was not different from baseline in the time-control
group. Compared with the respective baseline
Kfc
values, I/R-induced increases of
Kfc
were 80 ± 8% in the I/R-control
group and 30 ± 5% in the I/R-SuLa
group (P < 0.001).
P < 0.01 vs. I/R
control after I/R, *P < 0.001 vs.
I/R control at baseline, and
P < 0.001 vs.
I/R control group after I/R.
Hemodynamic measurements are shown in Table 1. Compared with baseline values, Ppa, Ppv, Ppc, Rpa, and Rpv did not vary after 3-h perfusion in the time-control group (Table 1). After I/R, Ppa was lower in the I/R-SuLa group compared with the I/R-control group. After I/R, Ppv, Ppc, Rpa, and Rpv were not different between the two groups (Table 1).
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After I/R, lung MPO activity in the I/R-control
group was higher than in the
time-control group (0.59 ± 0.04 vs. 0.32 ± 0.04 U/100 mg, respectively;
P < 0.01). In the I/R-SuLa
group, lung MPO activity after I/R was lower than in the
I/R-control group and not different
from lung MPO activity measured in the time-control group (Fig. 2).
P < 0.01 vs. I/R-control group.
During reperfusion, total WBC counts decreased similarly in both I/R groups (2,880 ± 163 and 2,700 ± 481 cells/µl before reperfusion vs. 1,900 ± 135 and 1,680 ± 246 cells/µl after reperfusion in the I/R-control and I/R-SuLa groups, respectively). Before reperfusion, blood PMN counts were 431 ± 41 and 404 ± 132 cells/µl in I/R-control and I/R-SuLa groups, respectively (NS). After I/R, the percentage decrease in blood PMN were similar in the I/R-control and I/R-SuLa groups (78 ± 5 and 87 ± 3% in the I/R-control and I/R-SuLa groups, respectively). During reperfusion, the variations of platelets, lymphocytes, monocytes, eosinophils, and basophil counts were not different between the two I/R groups.
An adhesion model was performed in vitro to confirm the
efficiency of SuLa in inhibiting interaction of PMN and endothelial cells. Results reported in Fig.
3 show that SuLa inhibited PMN adhesion to
TNF-- or CaI-stimulated endothelial cells by ~40%.
(TNF; 20 ng/ml) or calcium ionophore (CaI;
2.105 M) for 4 h and 15 min, respectively. Cells were then washed and incubated with saline
(SuLa) or Sula (SuLa+) (100 µM) for 15 min at 4°C.
Adherence was assessed as described in
METHODS;
n = 4 experiments; C, control
nonstimulated HUVEC. * P < 0.001 vs. saline-treated group.
DISCUSSION
This study shows that administration of the selectin ligand SuLa pentasaccharide attenuates the I/R-induced increase in lung microvascular permeability as well as the PMN accumulation in lung and reduces the adhesion of PMN to stimulated endothelial cells in vitro.
I/R lung injury is characterized by an increase in pulmonary microvascular permeability and a massive pulmonary PMN sequestration (1, 3, 6, 7). Because infiltrating PMN have been implicated as key mediators of the reperfusion-induced lung damages, isolated rat lungs were perfused with blood rather than with buffer. Moreover, to prevent lung injury due to ischemia-derived blood-borne products, the lungs were reperfused with fresh blood obtained from rat donors. Kfc was used to evaluate changes in lung microvascular permeability (22-24), and pulmonary sequestration of PMN during reperfusion was assessed by measuring lung MPO activity, which is a marker of tissue PMN infiltration (2, 16). In the time-control group, Kfc remained unchanged after 3 h of normal perfusion, thus demonstrating the stability of our preparation. As expected, in the I/R-control group, I/R-induced increase of Kfc and lung MPO activity after I/R were similar to those reported in our previous study (22).
A main step in the pathogenesis of I/R-induced lung injury is the adhesion of PMN to the vascular endothelium (19). Numerous studies conducted in various models of lung I/R consistently demonstrated that prevention of PMN adhesion by inhibition of leukocyte integrin component CD18 or endothelial cell adhesion molecule ICAM-1 improved reperfusion-induced lung injury (6, 7). One important property of the selectins is that they appear to be the initial adhesion molecules to influence the properties of PMN at the start of the inflammatory response (9, 10). Thus, selectins may serve as a target for therapeutic intervention in lung reperfusion injury. A recent study (26) indicates that survival after 6 h of lung reperfusion injury was improved by an antibody that binds and inhibits L- and E-selectins in intact sheep. However, the initial expression of lung reperfusion injury was not altered by blocking L- and E-selectins, suggesting that early lung injury induced by reperfusion was not dependent on L- and E-selectins (26). This was confirmed by a study in isolated rat lung, where monoclonal antibodies directed against P-selectin, but not those against L-selectin, protected the lungs against the I/R-induced permeability increase (15). Thus, contrary to P-selectin, L- and E-selectins would be projected to play only a minor role in the early phase of I/R lung injury.
One interesting aspect of selectins is that selectin-mediated adhesion
is dependent on carbohydrate binding. A plethora of simple and complex
carbohydrates have been reported to be recognized by the selectins
(29). The common feature of most of these carbohydrates is a
lactosamine backbone of either type 1 (Gal1-3GlcNAc) or type 2 (Gal1-4GlcNAc),
which are present in the blood group-related fucooligosaccharides
Lewisa and
Lewisx, respectively. Most of
these selectin-carbohydrate ligands carry sialylated, sulfated,
and/or fucosylated sequences (29). Knowledge of the
role of these carbohydrate ligands opens the possibility that bioactive
sugars can be developed to block one or more of the selectins in
selectin-dependent inflammatory injury. A recent study demonstrates
that sialyl Lewisx tri-
and tetrasaccharides administered intravenously had a protective effect
against an E-selectin-dependent acute lung injury induced by
intrapulmonary deposition of immune complexes containing immunoglobulin G (17). A P-selectin-dependent inflammatory lung injury induced by
cobra venom factor was similarly diminished by intravenous injection of
these oligosaccharides (18). More recently, administration of a
pentasaccharide analog of sialyl
Lewisx was demonstrated to
attenuate myocardial injury and PMN myocardial accumulation after 90 min of regional ischemia and 4.5 h of reperfusion (11). In the present
study, we have used the SuLa pentasaccharide, which was recently
synthetized by Lubineau et al. (14). In vitro binding studies indicate
that this pentasaccharide was a more potent ligand for E- and L-
selectins than the sialyl Lewisx
analogs (5, 30). Other studies suggested that such sulfated Lewisa analogs could also be
ligands for P-selectin (29). Accordingly, in our in
vitro study, SuLa induced a decrease in PMN adhesion to
endothelial cells stimulated by either CaI or TNF-, which have been
reported to induce expression of P-selectin and E-selectin respectively
(10, 29). Moreover, the present study demonstrates that this SuLa
pentasaccharide inhibits PMN-mediated lung reperfusion injury. Indeed,
compared with baseline values, SuLa induced a 68% inhibition of lung
injury and a virtually 100% inhibition in lung MPO content.
Interestingly, the circulating number of leukocytes decreased similarly after reperfusion in I/R-control and I/R-SuLa groups, whereas lung MPO activity was significantly lower in the treated group. Flushing the lungs with saline before determination of the lung MPO activity might account for this discrepancy. Flushing the lungs could have resulted in elimination of a significant part of the marginated PMN, leaving only firmly adherent PMN and/or PMN that have transmigrated through the endothelium. Taken together, all these observations suggest that SuLa inhibited not only PMN rolling but also PMN adhesion and/or transmigration. Although this hypothesis is presently purely speculative, various other sulfated polysaccharides have been shown to interfere strongly with leukocyte adhesion (8).
The development of selectin oligosaccharide ligands is attractive because of their lack of immune reactivity as well as their ease of handling for therapeutic use. Moreover, treatment with the SuLa pentasaccharide might effectively block the actions of all the selectins simultaneously, thus offering the advantage that it might protect the lung for longer periods of reperfusion. Additional studies in intact animals are necessary to confirm the applicability of this treatment.
In conclusion, we provide for the first time striking evidence that the SuLa pentasaccharide reduces lung PMN accumulation and adhesion to endothelial cells and exerts a significant degree of pulmonary protection in isolated rat lungs submitted to warm I/R.
ACKNOWLEDGEMENTS
We thank the medical staff of the Clinique Obstétricale de Fontenay aux Roses and of the Centre de Prélèvement de l'Hôpital Marie Lannelongue for providing the human umbilical cords and the human blood, respectively.
FOOTNOTES
Address for reprint requests: P. Hervé, Hôpital Marie Lannelongue, 133 Ave. de la Résistance, le Plessis Robinson, 92350 France.
Received 15 March 1996; accepted in final form 25 November 1996.
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