Circulation, Vol 84, 2154-2166, Copyright © 1991 by American Heart Association
AC Gasic, G McGuire, S Krater, AI Farhood, MA Goldstein, CW Smith, ML Entman and AA Taylor
BACKGROUND. Cytotoxic products of neutrophils (polymorphonuclear
leukocytes, PMNs) contribute to ischemia-reperfusion injury of several
tissues. Hydrogen peroxide (H2O2), one of the cytotoxic products of PMNs,
also promotes the adherence of PMNs to cultured vascular endothelial cells
in vitro. The present study was undertaken to determine if H2O2 also
augmented adhesion of PMNs to intact vessels perfused ex vivo and to
determine if H2O2-induced PMN adherence to intact canine carotid arteries
and external jugular veins or to cultured canine venous endothelium is
mediated by specific adherence ligands on the neutrophil and/or the
endothelium. METHODS AND RESULTS. Vessels were perfused for 20 minutes with
oxygenated Krebs-Henseleit bicarbonate buffer with and without H2O2, washed
with buffer alone, and then exposed to 111In-labeled isolated PMNs (10(7)
cells/vessel) under static conditions for up to 20 minutes before being
washed again. Residual radioactivity retained by the washed vessel was
counted as an index of PMN retention. The adherence of unlabeled PMNs to
cultured endothelial cells was determined by a visual assay method after
pretreatment of the endothelium with H2O2 for brief periods followed by
washing. Perfusion of vessels with H2O2 produced a transient,
concentration-dependent increase in PMN adhesion to both canine carotid
arteries and external jugular veins that was two to four times that of
control values at 1 mmol/l and declined at higher H2O2 concentrations. Peak
retention of PMNs by canine carotid arteries occurred 10 minutes after
exposure to 1 mmol/l H2O2 and then rapidly declined to control values; this
effect was replicated by a second 20-minute exposure of canine carotid
arteries to 1 mmol/l H2O2 60 minutes after the first exposure. Scanning and
transmission electron microscopy revealed not only adherence of PMNs to but
migration through the vascular endothelium of the carotid artery after H2O2
perfusion. The endothelium was intact in H2O2-treated arteries not exposed
to PMNs. H2O2-induced PMN retention was completely inhibited by addition of
catalase or the hydroxyl radical scavenger dimethylthiourea to the
perfusate by incubation of the PMN with a monoclonal antibody (Mab) against
CD18 (R15.7) or by perfusion of the H2O2-treated vessel with CL18/6, a Mab
against canine ICAM-1 (intercellular adhesion molecule-1). Similar effects
of Mabs on PMN adhesion to H2O2-pretreated cultured endothelium were noted.
The retention of PMNs by vessels mechanically denuded of endothelial cells
was markedly increased. H2O2 pretreatment of these vessels did not further
augment PMN adherence, and no inhibitory effect of R15.7 was noted.
Incubation of carotid arteries and PMNs with a specific platelet-activating
factor antagonist, WEB2086, completely inhibited the H2O2-induced increased
PMN retention by these vessels. CONCLUSIONS. These results indicate that
H2O2 in the absence of evidence for permanent endothelial cell injury, can
induce a transient, reversible, platelet-activating factor-dependent
adherence of PMNs to vessels by mechanisms that depend on an intact
endothelium and involve CD18 on the PMN and ICAM-1 on the endothelium.
ARTICLES
Hydrogen peroxide pretreatment of perfused canine vessels induces ICAM- 1 and CD18-dependent neutrophil adherence
Center for Experimental Therapeutics, Baylor College of Medicine, Houston, TX 77030.
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