(Circulation. 1997;95:1515-1522.)
© 1997 American Heart Association, Inc.
Articles |
Inhibition of Intimal Hyperplasia After Balloon Injury by Antibodies to Intercellular Adhesion Molecule-1 and Lymphocyte Function–Associated Antigen-1
From the Departments of Pathology II (H.Y., A.N., M.M.) and Internal Medicine III (T.I., H.M.), Kurume University School of Medicine, Kurume, Fukuoka 830, Japan.
Correspondence to Hideo Yasukawa, MD, Department of Pathology II, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka 830, Japan.
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Abstract |
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Background Although intercellular adhesion molecule-1 (ICAM-1) is known to be expressed in balloon-injured arteries, it remains unknown whether ICAM-1 plays a role in the progression of intimal hyperplasia (IH) induced by balloon injury.
Methods and Results We examined the ICAM-1 expression in rat carotid arteries at 1, 2, 5, 7, 10, and 14 days after injury by immunohistochemistry. Medial smooth muscle cells (SMC) expressed ICAM-1 intensely at 1 to 2 days after injury. The regenerating endothelial cells expressed ICAM-1 more than did those of intact carotid arteries. To investigate the effects of monoclonal antibodies (MAbs) on IH, we examined the intima/medial ratio of arteries at 2 weeks after injury in five treatment groups: nonimmune IgG, anti-membrane glycoprotein MAb, anti–lymphocyte function–associated antigen-1 (LFA-1) MAb, anti–ICAM-1 MAb, and anti–ICAM/LFA-1 MAb. Treatments were administered intravenously into rats for 6 consecutive days after injury. MAb against LFA-1 alone or membrane glycoprotein had no effect on IH. The intima/media ratios in anti–ICAM-1 MAb–treated and anti–ICAM-1/LFA-1 MAb–treated animals were significantly less than those in nonimmune IgG–treated and anti–membrane glycoprotein MAb–treated animals (P<.05).
Conclusions Balloon injury induced or upregulated the ICAM-1 expression on vascular SMC and on regenerating endothelial cells. MAb against ICAM-1 or ICAM-1/LFA-1 attenuated IH. These results suggest that ICAM-1 may play a role in the progression of IH after injury in rats.
Key Words: atherosclerosis • muscle, smooth • stenosis • angioplasty • remodeling
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Introduction |
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Intimal hyperplasia often causes clinically significant restenosis of arteries that have undergone therapeutic coronary interventions.1 2 This initial process is characterized by immune-mediated inflammatory reactions involving the migration of leukocytes, cytokine release, and secretion of growth factors at the site of injury.3 4 Through these reactions, vascular cells are activated with the expression of adhesion molecules, which have been suggested to play a contributory role in the pathogenesis of IH after vascular injury.5 6
ICAM-1 and LFA-1 are recently described ligand/receptor pairs of
adhesion molecules that play a critical role in the generation of
inflammatory or immune responses.7 8 9 10 LFA-1 is a member of
the integrin family found on most leukocytes. ICAM-1, a member of the
immunoglobulin supergene family, is expressed mainly on the surface of
EC and epithelial cells but not of SMC under normal conditions, whereas
its expression is induced or upregulated on vascular SMC and EC by
inflammatory cytokines such as interleukin-1, tumor necrosis
factor-
, and interferon-
.7 9 10 11 12 13
In atherosclerotic and balloon-injured arteries, expressions of ICAM-1 have been identified on EC and vascular SMC.14 15 16 17 18 However, it remains unknown whether ICAM-1 plays a causal role or is just an epiphenomenon in IH. Accordingly, we hypothesized that ICAM-1 may play a pivotal role in the progression of IH after balloon injury. To test this hypothesis, we examined the effects of MAbs against ICAM-1 and LFA-1 on IH after balloon injury in rats.
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Methods |
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Animals
Male Wistar rats weighing 240 to 260 g were obtained from Japan SLC Inc (Shizuoka, Japan). Animal care and treatment were conducted in conformity with institutional guidelines in compliance with international laws and policies (EEC Council Directive 86/609, OJL 358, December 1987; "Guide for the Care and Use of Laboratory Animals," NIH publication No. 85-23, 1985).
Balloon Injury
Rats were anesthetized through the intraperitoneal
administration of pentobarbital sodium (50 mg/kg). Rat carotid arteries
were denuded of the endothelium with a 2F Fogarty balloon embolectomy
catheter (Baxter Healthcare) that was introduced into the left common
carotid artery through the external carotid artery. The balloon was
inflated, and the catheter was retracted. This was repeated three
times, with the catheter turned 90° each time while it was retracted.
After removal of the catheter, the external carotid artery was ligated,
and the wound was closed.19 20 Endothelial denudation was
verified through staining with Evans blue (20 mg/kg) that had been
injected via the femoral vein of a subset of animals (n=10) 20 minutes
before they were killed.17
MAbs
MAb 1A29 (IgG1; Seikagaku Kogyo Co) against
rat ICAM-1 (CD54) and MAb WT.1 (IgG2a; Seikagaku Kogyo)
against rat LFA-1 (CD11a) were used in in vivo blocking studies that
has been previously described.21 22 23 Both antibodies
recognize a functional epitope and inhibit leukocyte adhesion to
endothelial monolayers in vitro.21 22 23 MAb MRC OX-2
(IgG1; SEROTEC Ltd) against membrane glycoprotein expressed
on arterial SMC24 25 was also used in an in vivo blocking
study to exclude the nonspecific effects of MAb that reacts with SMC.
We verified that this anti-membrane glycoprotein MAb could react with
cultured SMC from the rat aorta through the use of flow cytometric
analysis. (The MRC OX-2–positive cell rate was 88.76% when normal
mouse IgG was used as negative control.) Other MAbs were used for
immunohistochemical analysis: MAb Mar 1 (IgG1; Seikagaku
Kogyo) recognizes rat monocytes and macrophages26 ; MAb
R1-3B3 (mouse IgG2a; Seikagaku Kogyo) detects a 67-kD
single glycoprotein determinant present on rat thymocytes and
peripheral T lymphocytes27 ; and MAb 1A4
(IgG2a; Zymed Laboratories, Inc) reacts with the
-isoform of smooth muscle actin.28
Tissue Preparation and Immunohistochemistry
To evaluate the ICAM-1 expression immunohistochemically, 30 rats
were killed, and both carotid arteries were isolated from adherent
tissue at 1, 2, 5, 7, 10, and 14 days after balloon injury. After a
wash with phosphate-buffered saline and excision, the fresh samples
were immediately embedded in optimal cutting temperature (O.C.T.)
compound frozen through the use of dry ice acetone. Serial 6-µm-thick
frozen sections were adhered to poly-L-lysine–coated
slides and then fixed in cold acetone for 10 minutes. The labeled
streptavidin-biotin method was used for immunohistochemical staining as
described previously29 30 (LSAB Kit, DAKO Co). Briefly,
the specimens were treated with 3% hydrogen peroxide for 5 minutes to
inhibit endogenous peroxidase. All sections were incubated with 1%
bovine serum albumin and then incubated with primary antibodies (MAb
1A29, MAb Mar 1, MAb R1-3B3, and MAb 1A4) at room temperature for 30
minutes. After being washed three times in Tris-buffered saline (pH
7.4), biotinylated anti-mouse IgG secondary antibodies were applied,
followed by peroxidase-labeled streptavidin. Peroxidase activity was
visualized with the use of 3-amino-9-ethylcarbazole, and the sections
were faintly counterstained with Mayer's hematoxylin or methyl
green.
Antibody Treatment Study
Morphometry
To examine the effects of anti–ICAM-1 MAb and anti–LFA-1 MAb
on the progression of IH after balloon injury, 26 rats were assigned
randomly to one of five treatment groups: nonimmune IgG (group 1, n=6),
anti–membrane glycoprotein MAb (group 2, n=5), anti–LFA-1 (group 3,
n=5), anti–ICAM-1 MAb (group 4, n=5), or anti–ICAM-1 MAb/anti–LFA-1
MAb (group 5, n=5). Nonimmune IgG and MAbs were administered
intravenously to rats via the femoral vein at a dosage of 1 mg/kg (2
mg/kg in anti–LFA-1 alone–treated animals) of body weight per day for
6 consecutive days after balloon injury. This dosage has been shown to
suppress inflammatory cellular infiltration of experimental
uveitis31 and to prolong nerve allograft survival in
rats.32
Two weeks after balloon injury, carotid arteries were harvested as described above. After fixation in 4% paraformaldehyde, the specimens were embedded in paraffin, sectioned at 3-µm intervals, and stained with van Gieson's elastin staining. Three individual sections from the middle of injured lesions were examined morphometrically through videomicroscopy with the computerized digital image analysis system (NIH Image, National Institutes of Health) by an observer who was blinded to the group of samples. The intimal cross-sectional area was determined through subtraction of the area of the lumen from the area enclosed by the internal elastic lamina. The medial area was determined through subtraction of the area enclosed by the internal elastic lamina from the area enclosed by the external elastic lamina. The areas of the intima and of the media in three sections were averaged.33 Intraobserver variability of the intima/media ratio measurement was 2.2±0.5% for one slice (n=10).
Accumulation of Leukocytes
To examine the effects of MAb against ICAM-1 and LFA-1 on the
accumulation of monocytes/macrophages and T lymphocytes, we counted all
MAb Mar 1–labeled cells and MAb R1-3B3–labeled cells in the intima
and media 6 days after balloon injury.34
Statistical Analysis
All data are expressed as mean±SEM unless otherwise indicated.
Experimental groups were compared with the use of ANOVA and, when
appropriate, with Scheffé's test for multiple comparisons. A
value of P<.05 was considered significant.
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Results |
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Immunohistochemistry
Table 1
indicates the time course of ICAM-1
expression after balloon injury. In the uninjured rat carotid artery,
an endothelial monolayer and a medial layer remained intact, and the
expression of ICAM-1 was weakly positive on EC and negative on the
medial layer (Fig 1A). T lymphocytes labeled with MAb
R1-3B3 and monocytes/macrophages labeled with MAb Mar 1 were not
observed in intact arteries. At 1 and 2 days after the injury, although
no intimal thickening was observed, extensive medial SMC labeled with
MAb 1A4 (Fig 1B) intensely expressed ICAM-1 (Fig 1C), whereas sparse
monocytes/macrophages labeled with MAb Mar 1 were observed under the
internal elastic lamina in the medial layer. At 5 to 7 days after the
injury, regenerating EC and some SMC of the neointima moderately
expressed ICAM-1 (Fig 1D). At this stage, we observed some
monocytes/macrophages in the neointima and media (Fig 1E and Table 2). At 10 days after balloon injury, ICAM-1 expression
on the medial SMC was absent, whereas regenerating EC still moderately
expressed ICAM-1 (Fig 1F). During the entire experiment, only a few MAb
R1-3B3–positive cells were observed.
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Antibody Treatment Study
There was no significant difference in body weight between
MAb-treated animals and control animals at 2 weeks after balloon injury
(group 1, 290±3 g; group 2, 288±4 g; group 3, 291±5 g; group 4,
285±6 g; group 5, 289±4 g; P=NS). We did not find any
other evidence indicating toxicity of MAb administrations. Fig 2 is a representative photomicrograph of cross sections
of rat carotid arteries at 2 weeks after balloon injury. The intima of
the uninjured right carotid arteries remained intact, consisting of a
monolayer of EC only (Fig 2A). Balloon injury induced marked IH in
nonimmune IgG–treated control animals (group 1; Fig 2B) and in
anti-membrane glycoprotein–treated animals (group 2; Fig 2C), whereas
anti–ICAM-1 MAb alone (Fig 2E) or in combination with anti–LFA-1 MAb
treatment (group 5; Fig 2F) markedly reduced IH compared with control
animals (group 1). Anti–LFA-1 at 2 mg/kg did not affect IH (Fig 2D).
In morphometric analysis, significant decreases in the neointimal
cross-sectional area and the intima/media ratio were noted in animals
treated with anti–ICAM-1 MAb alone (group 4) or in animals treated
with anti–ICAM-1 MAb in combination with anti–LFA-1 MAb (group 5)
compared with control animals (group 1), whereas either membrane
glycoprotein MAb or anti–LFA-1 MAb alone did not affect neointimal
cross-sectional area and intima/media ratio (Fig 3).
There were no statistical differences among control, anti-membrane
glycoprotein–treated, and anti–LFA-1–treated animals in the
neointimal cross-sectional area and intima/media ratio. The medial
cross-sectional area did not differ significantly among the five groups
(group 1, 0.118±0.004 mm2; group 2, 0.124±0.009
mm2; group 3, 0.126±0.006 mm2; group 4,
0.118±0.004 mm2; group 5, 0.123±0.001
mm2; P=NS).
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Table 2
shows the percent of accumulation of monocytes/macrophages
labeled with MAb Mar 1 in all counted cells at 6 days after balloon
injury. There was no accumulation of the monocytes/macrophages in
uninjured arteries, whereas the balloon injury resulted in a
significant accumulation in the neointima and media. However, either
anti–ICAM-1 MAb or the combination of anti–ICAM-1 and anti–LFA-1 MAb
did not attenuate the accumulation of monocytes/macrophages in the
balloon-injured arteries statistically (Table 2). Because lymphocyte
accumulation was sparse, no effects of MAb treatment were observed in
the lymphocyte accumulation (data not shown).
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Discussion |
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In the present study, we demonstrated that balloon injury induced the high level of ICAM-1 expression on both SMC and regenerating EC in rat carotid arteries. Furthermore, anti–ICAM-1 MAb alone or anti–ICAM-1 MAb in combination with anti–LFA-1 MAb significantly attenuated IH when administered systemically for 6 consecutive days and immediately after balloon injury. These results suggest that ICAM-1 may play an important role in the development of IH after balloon injury in rats.
Time Course of ICAM-1 Expression
Leukocytes have been shown to accumulate at the site of
injury,17 35 and it has been suggested that adhesion
molecules may contribute to the recruitment of these cells at
balloon-injured arteries.6 Tanaka et al17 18
demonstrated the temporal expression of inducible cell-surface adhesion
molecules on both EC and SMC after balloon injury in the rabbit aorta.
They demonstrated that compared with the uninjured endothelium,
regenerating EC showed high levels of ICAM-1 expression early after
balloon injury, which lasted for 30 days after balloon injury. The
expression of ICAM-1 on the neointimal SMC was absent at 2 days,
moderate at 5 days, and intense at 10 days after balloon
injury.17 18 They did not observe the expression of ICAM-1
on the media throughout the experimental periods. In contrast to their
findings, we demonstrated the early (1 to 2 days) and intense
expression of ICAM-1 on the medial SMC after balloon injury in the rat
carotid model. Although the reason for this difference remains unknown,
it might have been due to the species difference and/or the site of
vessels examined. The expression of ICAM-1 on the medial SMC became
less intense at 5 to 7 days and absent at 10 days after balloon injury.
It is interesting to note that the expression of ICAM-1 on the
neointimal SMC became positive as the expression of ICAM-1 of the
medial SMC was fading out at 5 to 7 days after balloon injury. The
expression of ICAM-1 on the regenerating EC in this study was similar
to that in the previous report. Although the meanings and mechanisms of
the temporal and spatial expression of ICAM-1 on the regenerating EC,
neointimal SMC, and medial SMC are unclear, our results may suggest an
important link between the expression of ICAM-1 and IH after balloon
injury in the rat carotid artery.
Effects of Monoclonal Antibodies
Recently, in vitro studies have shown that the ICAM-1/LFA-1
interaction is critical in immune-mediated inflammatory
reactions.7 8 9 10 In in vivo studies, the blockade of
ICAM-1/LFA-1 pathway by MAbs against ICAM-1 and LFA-1 has been shown to
reduce the disease activity of rat experimental crescentic
glomerulonephritis,36 murine cardiac allograft
rejection,37 rat adjuvant arthritis,38 and
rat myocardial reperfusion injury.39 Because ICAM-1 was
highly induced on the medial SMC and upregulated on the regenerating EC
within 7 days after balloon injury in our study, we administered MAbs
or nonimmune IgG for the first 6 days after balloon injury. Nonimmune
IgG had no effect on IH induced by balloon injury. IH induced by
balloon injury was significantly attenuated by systemic administrations
of anti–ICAM-1 MAb alone or of anti–ICAM-1 MAb in combination with
anti–LFA-1 MAb and there were no adverse effects. A recent study
suggests that any antibody that reacts with SMC in vivo may inhibit SMC
migration.40 However, this possibility was unlikely
because anti-membrane glycoprotein MAb, which binds SMC surface
antigen, did not affect IH. These results may suggest that ICAM-1 plays
an important role in IH after balloon injury in the rat carotid
artery.
It has been shown that anti–ICAM-1 MAb and anti–LFA-1 MAb have synergistic or additive effects on various pathophysiological states, such as experimental glomerulonephritis,36 cardiac allograft rejection,37 and autoimmune diabetes.41 In addition, it has been shown in some animal models17 42 but not in others43 44 that lymphocytes accumulate in the neointima of the balloon-injured arteries. These results may suggest that lymphocytes are involved in IH when ICAM-1 is expressed on the vessels. In the present study, however, we observed little accumulation of lymphocytes in the neointima throughout the experiment. Moreover, anti–LFA-1 MAb alone did not affect IH, and anti–LFA-1 MAb in combination with anti–ICAM-1 MAb did not produce any additive or synergistic effects on IH compared with the use of anti–ICAM-1 MAb alone. Thus, our results may suggest a dispensable role of lymphocytes in IH in the rat balloon injury model.
Possible Mechanisms of Attenuation of IH
There are several potential mechanisms of the antiproliferative
effects of anti–ICAM-1 MAb on the progression of IH in this rat model.
First, anti–ICAM-1 MAb may have inhibited monocytes transmigration
through the regenerating EC, which expressed upregulated ICAM-1 after
balloon injury. In fact, several previous investigators reported that
vascular EC that expressed ICAM-1 and monocytes/macrophages were
identified in atherosclerotic14 15 16 and
balloon-injured17 18 arteries. Chemotaxis and recruitment
of monocytes have been considered to be critical events in the
restenosis after coronary angioplasty in humans.3 In this
scenario, monocytes adhere to the site of the injury, accumulate into
the vessel wall, and stimulate the migration of medial SMC to the
intima in the balloon-injured artery. Activation of
monocytes/macrophages results in the release of key mediators of
inflammatory reactions, such as interleukin-1, tumor necrosis
factor-, platelet-activating factor, and superoxide.3
Guzman et al45 reported that the inhibition of monocyte
chemoattraction with monocyte chemotactic protein antibody decreased
neointimal proliferation after vascular injury in a rabbit model.
Furthermore, Takahashi et al46 reported that MAbs against
ICAM-1 and LFA-1 inhibited monocytes transmigration through the
activated endothelium with upregulated ICAM-1 expression by
interleukin-1ß in vitro. Thus, it has been suggested that ICAM-1 may
play a role in the accumulation of monocytes/macrophages in the vessel
wall. However, our results are not consistent with the hypothesis that
increased expression of ICAM-1 leads to increased transendothelial
migration of monocytes/macrophages into the vessel because we have
shown that anti–ICAM-1 MAb treatment attenuated IH without influencing
the number of monocytes/macrophages in the vessel wall.
Second, although several investigators reported that SMC that expressed
ICAM-1 and monocytes/macrophages were identified in
atherosclerotic14 15 16 and balloon-injured17
arteries, little is known about the signal transduction between SMC and
monocytes/macrophages through ICAM-1/LFA-1 pathway. An in vitro
experiment showed that anti–ICAM-1 MAb inhibited monocyte adhesiveness
to cultured vascular SMC in which ICAM-1 expression was induced by
tumor necrosis factor-.12 In addition, recent evidence
showed that macrophage inflammatory protein-1 production was induced
in monocytes cultured on ICAM-1–coated plates,47
suggesting that intercellular signaling via ICAM-1 pathway plays an
important role in cytokine production of monocytes/macrophages.
Therefore, it is possible that ICAM-1 MAb interferes not only with cell
adhesion but also with intercellular signaling between
monocytes/macrophages and vascular SMC and may have attenuated IH in
rat balloon-injured artery.
Third, it has been reported that expression of ICAM-1 on SMC may be relevant to the phenotypical change of SMC.11 12 15 This phenotypical change of SMC is considered to be essential to the migration of SMC from media to intima during vascular regeneration after balloon injury.48 In addition, the migration of SMC from the media to intima occurs at an early phase after balloon injury and critically contributes to the progression of IH.49 In support of this hypothesis, we demonstrated that ICAM-1 was highly expressed and expressed early on the media and that MAb against ICAM-1 significantly attenuated the IH. Thus, it is possible that anti–ICAM-1 MAb may have inhibited the SMC migration from the media into the intima. However, this possibility remains to be elucidated.
Study Limitations
In the present study, we observed the development of IH within 14
days after balloon injury. It has been demonstrated that after balloon
injury, SMC migration and proliferation occur within the first 2
weeks.19 20 Subsequent modest thickening is the result of
connective tissue synthesis and accumulation by activated
SMC.19 20 Therefore, it is assumed that the major process
of IH occurs within the first 2 weeks. However, we still could not
conclude in this study whether anti–ICAM-1 MAb delayed or prevented
IH. This should be examined by analyzing the results at 21 to 28 days
after balloon injury. We investigated the effect of rat anti–ICAM-1
MAb in this experiment because rat ICAM-1 has been cloned and the
specificity of anti–ICAM-1 MAb has been verified.21
However, because another ICAM family for rat has not been cloned and is
not presently available, we could not examine the cross reaction with
another ICAM family member. This possibility should be elucidated.
In summary, we demonstrated that balloon injury induced high levels of ICAM-1 expression on SMC and regenerating EC in rat carotid arteries and that anti–ICAM-1 MAb alone or the combination with anti–LFA-1 MAb significantly attenuated IH after balloon injury. Our results suggest that ICAM-1 is possibly involved in the pathogenesis of IH after balloon injury in rats.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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We thank Mayumi Miura, Keiko Sato, and Nayumi Toyota for their technical assistance.
Received September 11, 1996; revision received November 4, 1996; accepted November 14, 1996.
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