(Circulation. 1997;95:981-987.)
© 1997 American Heart Association, Inc.
Articles |
Evidence for the Rapid Onset of Apoptosis in Medial Smooth Muscle Cells After Balloon Injury
the Division of Cardiovascular Research, St Elizabeth's Medical Center, Tufts University School of Medicine (H.P., L.M., K.K, K.W.), and the Program in Cell, Molecular, and Developmental Biology, Sackler School of Biomedical Sciences, Tufts University (H.P., K.W.), Boston, Mass.
Correspondence to Kenneth Walsh, Division of Cardiovascular Research, St Elizabeth's Medical Center, 736 Cambridge St, Boston, MA 02135-2997. E-mail kwalsh@opal.tufts.edu.
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Abstract |
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Background Vascular myocyte apoptotic cell death has been reported in human atherectomy and endarterectomy specimens and for neointimal smooth muscle cells (SMCs) in balloon-injured rat carotid arteries between 7 and 30 days after injury. However, the immediate effect of balloon injury on medial SMC viability has not been examined.
Methods and Results Rat carotid arteries were harvested at the time of balloon injury (T=0) and at 0.5, 1, 2, and 4 hours after injury. Uninjured vessels or vessels harvested at the time of injury (T=0) did not display evidence of apoptosis. However, as early as 30 minutes after injury, 70% of medial SMCs appeared apoptotic by TdT-mediated dUTP nick end labeling (TUNEL) analysis and by the appearance of condensed chromatin. High frequencies of TUNEL-positive cells were also observed at 1 and 2 hours after injury but not at 4 hours. Transmission electron microscopy revealed many cells with morphological characteristics of apoptosis in the injured sections. A marked decrease in bcl-X expression was detected in the most luminal layers of the media. To corroborate these findings in a second animal model, rabbit external iliac arteries were analyzed after balloon angioplasty. Apoptotic cell death was evident in rabbit arteries at 30 minutes and at 4 hours after injury.
Conclusions As early as 30 minutes after balloon injury, myocytes appear to undergo apoptotic cell death at a high frequency as shown by TUNEL staining, chromatin condensation, and the appearance of morphological features in electron micrographs. The induction of apoptosis coincides with a marked downregulation of bcl-X expression.
Key Words: balloon • apoptosis • angioplasty • muscle, smooth • remodeling
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Introduction |
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Apoptosis, a noninflammatory mechanism of cell elimination, involves cytoplasmic shrinkage, maintenance of membrane integrity, DNA fragmentation and condensation, and the formation of apoptotic bodies.1 2 The apoptotic process is rapid and can be completed within 34 minutes in vivo, as demonstrated by time-lapse cinematography.3 4 In contrast, necrotic cell death occurs when cells swell and expunge their contents into the extracellular environment, thereby eliciting an inflammatory response.5 The discovery of families of apoptotic regulatory genes has led to the hypothesis that the relative stoichiometries of apoptotic accelerator and inhibitory proteins function as molecular rheostats that control cell survival.6 The regulation of these genes by exposure to chemical treatment, growth factor removal, or mechanical stress is a key determinant of cell fate.7 8
Balloon injury of the vessel wall results in stresses that include the destruction of the endothelium and the stretching of the medial smooth muscle cells (SMCs). The proliferative responses of vascular SMCs to balloon injury have been well characterized in a number of animal models.9 10 11 12 13 14 In injured rat carotid arteries, DNA synthesis in SMCs peaks at 48 hours, whereas the total accumulation of SMCs in the neointima reaches a maximum at 2 weeks after injury. However, continuous cellular proliferation occurs for up to 12 weeks with no discernible increase in SMC number. The death of neointimal SMCs was proposed to account for the lack of SMC accumulation at these later time points.9 Consistent with this hypothesis, recent investigations have demonstrated that SMC apoptosis occurs in the neointima from 7 to 30 days after injury.15 16 Using TdT-mediated dUTP nick end labeling (TUNEL) as an indicator of apoptosis, a maximum of 40% apoptotic cell death was observed in the neointima at 9 days after injury.15 In another study using in situ end labeling, a technique similar to TUNEL that uses DNA polymerase I instead of terminal deoxynucleotidyl transferase revealed a maximum of 14.3±0.3% apoptotic cell death in the neointima 20 days after injury.16 In addition to in situ end-labeling positivity, the apoptotic phenotype was confirmed by identification of morphological structures that are characteristic of apoptosis by transmission electron microscopy. In both studies, little or no apoptosis was observed in the medial SMCs, and the effect of balloon injury at early time points was not investigated.
Here, we investigated the effects of balloon injury on medial SMC viability at several early time points. In rat carotid and rabbit external iliac arteries, balloon injury induced SMC apoptosis within 30 minutes, as indicated by positive TUNEL staining, chromatin condensation, and the presence of characteristic morphological features using transmission electron microscopy. These data suggest that the rapid onset of medial SMC apoptosis is a prominent cellular response to vascular injury.
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Methods |
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Rat and Rabbit Models of Arterial Lesion Formation
The rat carotid model of balloon injury used in this study was based on that of Clowes et al.9 10 Male Sprague-Dawley rats (n=4 for each time point) were anesthetized with an injection of sodium pentobarbital (45 mg/kg IP, Abbot Laboratories). In anesthetized rats, the neck area was prepared aseptically, and the bifurcation of the left common carotid artery was exposed through a ventral midline incision. A 2F Fogarty embolectomy catheter (Baxter Edwards Healthcare Corp) was introduced into the external carotid artery and advanced to the distal ligation of the common carotid artery. The balloon was inflated with saline, drawn toward the arteriotomy site, and pulled back three times to denude the endothelium. The arteriotomy was tied off with a 2-0 silk suture, and the subcutis was closed with a 3-0 silk suture. Antibiotics (0.1 mL Di-trim SC) were given immediately after surgery. Rats were killed at various times after surgery (0, 0.5, 1, 2, 4, and 8 hours after injury). The injured left and uninjured right common carotid arteries were immediately excised and divided into two populations: one was fixed in 4% paraformaldehyde, and the other was fixed in methanol. Arterial segments were then embedded in paraffin, cut into longitudinal (5-µm) sections, and assessed by TUNEL and Hoechst 33258 staining. Nuclear density was calculated in multiple sections by counting the number of nuclei per area on a slide stained with hematoxylin and eosin. To provide a positive control for TUNEL, male rats were surgically castrated and killed 3 days after castration. The ventral prostates were harvested and immediately placed in liquid nitrogen. Frozen sections (5 µm) were cut and analyzed by TUNEL.
For the rabbit model of balloon angioplasty (n=4), a 20-mm-long channel balloon angioplasty catheter (Boston Scientific Corp) was introduced through the right carotid artery over a 0.014-in guidewire under fluoroscopic guidance and advanced into the abdominal aorta. A baseline angiogram was performed after a single intra-arterial bolus of 200 mg isosorbide dinitrate after interposition of a calibrated grid for computation of the enlargement factor. The balloon angioplasty catheter was advanced into the external iliac artery and then inflated three times for 1-minute periods at a nominal pressure of 6 atm. The balloon was deflated for 1 minute between each inflation. The size of the balloon was chosen to achieve a 1.4:1 to 1.5:1 balloon-to-artery ratio. The noninjured contralateral iliac artery was used as a control. The animals were killed with an overdose of pentobarbital at 30 minutes or 4 hours after the balloon angioplasty procedure. Sections of iliac arteries were removed, washed in PBS, and immersion-fixed in a 4% solution of paraformaldehyde. Arterial segments were then embedded in paraffin, cut into longitudinal sections, and assessed. Tissue sections (5 µm) were also stained with hematoxylin and eosin after deparaffinization and rehydration for conventional light microscopic analysis.
The animal protocols used in this study were approved by the Institutional Animal Care and Use Committee of St Elizabeth's Medical Center, and they complied with the Guide for the Care and Use of Laboratory Animals (National Institutes of Health publication 86-23, revised 1985).
TUNEL and Nuclear Condensation
The 4% paraformaldehyde–fixed sections (5 µm) were deparaffinized and rehydrated. The tissue was permeabilized with 20 mg/mL proteinase K for 30 minutes. Terminal deoxynucleotidyl transferase enzyme and dUTP conjugated to a fluorescein cocktail were added to the tissue sections according to the manufacturer's specifications (Boehringer Mannheim in situ death detection kit). Nuclei were counterstained with Hoechst 33258 (Sigma) and mounted for examination with mounting media for fluorescence (Kirkegaard & Perry Laboratories, Inc). Specimens were examined and photographed on a Diaphot microscope (Nikon Inc) equipped with a phase-contrast and epifluorescence optics (x100) lens. Pictures were recorded on Kodak Gold Plus film (Eastman Kodak Co). The percentages of apoptotic nuclei were calculated by determining the number of Hoechst-stained nuclei that were positive for TUNEL staining (n=4 arteries per time point). Approximately 100 nuclei were counted for each section.
Transmission Electron Microscopy
Rat and rabbit uninjured arteries, 30 minutes and 4 hours after injury, were excised and fixed in 2.5% glutaraldehyde, 4% paraformaldehyde, and 0.1 mol/L sodium cacodylate. Sections were postfixed in 1% osmium tetroxide, dehydrated, stained en bloc with 3% uranyl acetate and Sato lead stain, and embedded in epoxy resin (Epon 812). Thin sections were examined with a Philips CM-10 electron microscope.
Immunohistochemistry
Five-micrometer sections from uninjured and injured rat arterial tissue fixed in methanol were deparaffinized and blocked in 10% goat serum. Sections were incubated with rabbit polyclonal anti–bcl-X antibody (Santa Cruz) or rabbit polyclonal anti-bax antibody. Peptide competitions were performed on each section using control peptides at 10 times the concentration of the antibody. Prostates from rats 3 days after castration were used as a positive control. Sections were then washed and incubated with biotinylated goat anti-rabbit antibody. Streptavidin conjugated to alkaline phosphatase was then added to the sections. Signals were determined with the addition of fast red substrate. Sections were counterstained with hematoxylin to visualize nuclei.
Statistical Analysis
All results are expressed as mean±SEM. Statistical significance was evaluated with a two-tailed unpaired Student's t test for comparisons between the means of two groups. A value of P<.05 was interpreted to denote statistical significance.
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Results |
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TUNEL Analysis of Balloon-Injured Rat Carotid Arteries
The TUNEL procedure stains nuclei that contain nicked DNA, a characteristic exhibited by cells in the early stages of apoptotic cell death. An immunofluorescent TUNEL analysis was performed on sections from uninjured and injured rat carotid arteries. Uninjured arteries and arteries harvested immediately after injury (T=0) had no detectable TUNEL-positive nuclei. However, a large number of TUNEL-positive nuclei were detected in the layers of the media closest to the lumen at 30 minutes after injury (Fig 1A
). At 1 hour after injury, a high level of TUNEL-positive nuclei were also detected, but by 2 hours the number of TUNEL-positive cells appeared to decline dramatically. Sections prepared from carotid arteries 4 hours after injury had few detectable positive nuclei. To verify that the intensity of the TUNEL-positive staining was consistent with apoptosis in these arterial segments, rat ventral prostates (3 days after castration) were stained by identical methods. Surgical castration has previously been shown to induce regression of the rat ventral prostate and to induce 85% of the ventral prostate cells to undergo apoptosis.17 The TUNEL-positive signals detected in the arterial sections were similar if not identical to that seen in the 3-day-postcastration rat ventral prostates (not shown). TUNEL-positive nuclei were not detected in adventitial cells at any of the time points examined in this study. Higher magnification of Hoechst-stained arterial sections revealed intensely fluorescent nuclei, which is indicative of chromatin condensation, corresponding to the TUNEL-positive nuclei (Fig 1B).
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The percentage of TUNEL-positive nuclei in four rat arterial segments per time point were determined by comparing the numbers of TUNEL-positive and Hoechst-positive nuclei (Fig 2). At 30 minutes after injury, 70±4% of the medial vascular SMCs were TUNEL-positive. At 1 hour and 2 hours after injury, 55±12% and 8±6% of nuclei were TUNEL-positive, respectively. Few or no TUNEL-positive nuclei were detected in the uninjured control vessels, in vessels immediately after injury (T=0), or in vessels at 4 hours after injury. Under the balloon injury conditions used here, we observe a 1.6±0.14:1 intima-to-media ratio and a 42±4% luminal narrowing at 2 weeks after injury (not shown).
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TUNEL Analysis of Rabbit Iliac Arteries After Balloon Angioplasty
TUNEL analysis was also performed on tissue sections from uninjured rabbit external arteries and arteries harvested from rabbits at 0.5 and 4 hours after injury. Similar numbers of TUNEL-positive nuclei were detected in the rabbit arteries at 0.5 hour (Fig 3) and 4 hours after injury (not shown), but no TUNEL-positive cells were detected in the uninjured vessels (Fig 3). At either of these postinjury time points, the rabbit iliac arterial sections displayed lower frequencies of TUNEL-positive cells than the 0.5 or 1 hour postinjury sections of rat carotid artery (compare Figs 1A and 2
). This lower frequency of TUNEL-positive cells may be due to species or procedural differences.
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Transmission Electron Microscopy of Rat and Rabbit Arterial Sections
Transmission electron microscopy was performed on uninjured, 0.5 hour postinjury, and 4 hours postinjury arterial sections from rat and rabbit arteries. Rat carotid arteries harvested at 30 minutes after injury contained many cells with condensed chromatin and cytoplasmic shrinkage, whereas the organelle membranes appeared intact (Fig 4A versus 4B). Similar to the uninjured rat arterial sections, sections from uninjured rabbit arteries contained SMCs with normal-appearing nuclei and no detectable cytoplasmic shrinkage (Fig 4C). At 0.5 hour after injury, SMCs closest to the lumen displayed chromatin condensation that was localized to the edges of the nuclear membrane (not shown). At 4 hours after injury, more dramatic changes in the rabbit SMC nuclei were observed, including budding of condensed chromatin (Fig 4D). The formation of cytoplasmic vacuoles, the result of cytoplasmic shrinkage, was also evident, whereas organelle membranes did not display an altered morphology. The adventitial cells in the injured rat and rabbit arteries did not display apoptotic morphologies (not shown).
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Immunohistochemistry Using Anti–bcl-X and Anti-bax Antibodies
Rat injured and uninjured carotid arterial sections were analyzed for bcl-X and bax expression. Previous immunohistochemical analyses have shown that the bcl-X protein, which protects against apoptosis, is highly expressed in vascular smooth muscle.18 The bax protein, an apoptotic accelerator, is also highly expressed in vascular smooth muscle.19 Consistent with previous reports, uninjured rat SMCs display intense bcl-X staining (Fig 5). At 1 hour after injury, however, the intensity of bcl-X staining decreased, and the downregulation was particularly evident in the most luminal layers of the injured media (Fig 5), the same layers that displayed the most TUNEL-positive nuclei (Fig 1A). In contrast, the intense bax immunostaining did not appear to change on injury (not shown). Antibody specificity for bax and bcl-X was indicated by the complete loss of signal when a molar excess of immunogenic peptide was preincubated with the appropriate antibody (not shown).
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Discussion |
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Apoptotic cell death has been documented in human atherectomy and endarterectomy specimens by TUNEL and electron microscopic data.20 21 22 These observations suggest that cell death may be a feature that influences the size and stability of human vessel wall lesions. Previous studies in the rat carotid model of balloon injury demonstrated that apoptotic SMC death occurs in the neointima from 7 to 30 days after injury.15 16 Here, we provide data indicating that a high frequency of medial SMC apoptosis occurs soon after the balloon injury of rat carotid and rabbit external iliac arteries. Apoptosis in medial SMCs was indicated by positive TUNEL and by the high intensity of the Hoechst 33258 nuclear stain, which is caused by the condensation of chromatin. Further evidence for the apoptotic phenotype was provided by transmission electron microscopy, which revealed intact organelles, cell shrinkage, and the formation of condensed chromatin.
In rat carotid arteries, the incidence of TUNEL-positive SMCs in the medial layer was 70±4% at 30 minutes after injury and 55±12% at 1 hour after injury. The incidence of TUNEL fell to 8±6% at 2 hours after injury and <1% at 4 hours after injury. This time course of TUNEL-positivity suggests that the medial SMC population responds uniformly to the balloon injury and that the cells are rapidly eliminated, either through phagocytosis or by extrusion into the lumen. Consistent with this hypothesis, we determined that a 65% loss in cellular density in the media (P<.004) had occurred as early as 4 hours after injury (not shown). Previously it had been reported that balloon injury produces a 25% loss of medial SMCs in rat carotid arteries at 24 hours after injury and a 35% to 40% loss in DNA content of medial cells in rabbit iliac arteries at 20 hours after injury.9 12 23 These reported losses of medial cellularity and DNA content are consistent with our observations of apoptotic cell death at early time points. However, at the later time points, significant DNA synthesis and presumably cell division9 and cell migration24 may have occurred, leading to an underestimation of cell loss. The decrease in bcl-X staining intensity on injury, especially in the most luminal layers of the media, which also exhibit the greatest number of TUNEL-positive nuclei, suggests that modulations in the level of this protein may be a feature of the apoptotic response to injury. It has been postulated that bcl-X confers protection from apoptosis by binding to bax protein and thereby prevents the formation of bax homodimers, which promote apoptosis.6 Thus, the reduction of bcl-X in injured arteries may permit bax to form homodimers, leading to the acceleration the apoptotic process.
The findings reported here may have consequences on the development of strategies to deliver genes to the vessel wall to treat restenosis and other vascular diseases.25 26 The upper medial layers of SMCs are most likely to be transduced by the prospective genes that are delivered to the lumen of the artery. These same cells are probably most susceptible to apoptosis in response to the mechanical stresses of balloon angioplasty. Thus, the luminal SMC layers may function as a barrier to the transduction of SMCs in the deeper layers, and it is these deeper cells that are likely to give rise to the daughter cells that repopulate the media. These features may contribute to the low transduction efficiencies that have been reported for the localized delivery of genes to the arterial wall.27 28
The distension of the vessel wall by balloon angioplasty is likely to disrupt integrin–matrix protein interactions. It has been demonstrated that SMC proliferation is induced by mechanical strains that are sensed by integrin–matrix protein interactions.29 It has also been shown that integrin ligation events are critical for the survival of proliferating vascular cells during angiogenesis.30 Thus, it is conceivable that the rapid, injury-induced apoptosis described here is a consequence of a cellular response to proliferative signals when normal cell-matrix interactions have been perturbed. Although the specific links between cell cycle control and cell survival are largely unknown, aspects of this regulation have been elucidated in myocytes that terminally differentiate.31 32 Thus, it will be of interest to determine the molecular mechanism by which the myocytes of the vessel wall coordinate proliferation and apoptosis in response to acute balloon injury.
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Acknowledgments |
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This work was supported by NIH grants AR-40197 and HL-50692 to Dr Walsh. Dr Maillard was supported by the French Federation of Cardiology. The authors thank Jim Barry and Boston Scientific Corporation for providing catheters. We gratefully acknowledge Marianne Kearney and Jeffrey M. Isner for advice and helpful discussions.
Received July 2, 1996; revision received September 20, 1996; accepted September 30, 1996.
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D. K. Jagadeesha, T. E. Lindley, J. DeLeon, R. V. Sharma, F. Miller, and R. C. Bhalla Tempol therapy attenuates medial smooth muscle cell apoptosis and neointima formation after balloon catheter injury in carotid artery of diabetic rats Am J Physiol Heart Circ Physiol, September 1, 2005; 289(3): H1047 - H1053. [Abstract] [Full Text] [PDF]
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T. Nakazawa, T. Chiba, E. Kaneko, K. Yui, M. Yoshida, and K. Shimokado Insulin Signaling in Arteries Prevents Smooth Muscle Apoptosis Arterioscler. Thromb. Vasc. Biol., April 1, 2005; 25(4): 760 - 765. [Abstract] [Full Text] [PDF]
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 H. Li, S. Telemaque, R. E. Miller, and J. D. Marsh High Glucose Inhibits Apoptosis Induced by Serum Deprivation in Vascular Smooth Muscle Cells via Upregulation of Bcl-2 and Bcl-xl Diabetes, February 1, 2005; 54(2): 540 - 545. [Abstract] [Full Text] [PDF]
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J. Cornelissen, J. Armstrong, and C. M. Holt Mechanical Stretch Induces Phosphorylation of p38-MAPK and Apoptosis in Human Saphenous Vein Arterioscler. Thromb. Vasc. Biol., March 1, 2004; 24(3): 451 - 456. [Abstract] [Full Text]
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N. Beohar, J. D. Flaherty, C. J. Davidson, R. C. Maynard, J. D. Robbins, A. P. Shah, J. W. Choi, L. A. MacDonald, J. P. Jorgensen, J. V. Pinto, et al. Antirestenotic Effects of a Locally Delivered Caspase Inhibitor in a Balloon Injury Model Circulation, January 6, 2004; 109(1): 108 - 113. [Abstract] [Full Text] [PDF]
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A. Forte, S. Esposito, M. De Feo, U. Galderisi, C. Quarto, F. Esposito, A. Renzulli, L. Berrino, M. Cipollaro, L. Agozzino, et al. Stenosis progression after surgical injury in Milan hypertensive rat carotid arteries Cardiovasc Res, December 1, 2003; 60(3): 654 - 663. [Abstract] [Full Text] [PDF]
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 E. Stabile, Y. F. Zhou, M. Saji, M. Castagna, M. Shou, T. D. Kinnaird, R. Baffour, M. D. Ringel, S. E. Epstein, and S. Fuchs Akt Controls Vascular Smooth Muscle Cell Proliferation In Vitro and In Vivo by Delaying G1/S Exit Circ. Res., November 28, 2003; 93(11): 1059 - 1065. [Abstract] [Full Text] [PDF]
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K. Stephenson, J. Tunstead, A. Tsai, R. Gordon, S. Henderson, and H. M. Dansky Neointimal Formation After Endovascular Arterial Injury Is Markedly Attenuated in db/db Mice Arterioscler. Thromb. Vasc. Biol., November 1, 2003; 23(11): 2027 - 2033. [Abstract] [Full Text] [PDF]
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F. J. Schaub, W. C. Liles, N. Ferri, K. Sayson, R. A. Seifert, and D. F. Bowen-Pope Fas and Fas-Associated Death Domain Protein Regulate Monocyte Chemoattractant Protein-1 Expression by Human Smooth Muscle Cells Through Caspase- and Calpain-Dependent Release of Interleukin-1{alpha} Circ. Res., September 19, 2003; 93(6): 515 - 522. [Abstract] [Full Text] [PDF]
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T. Tokunou, R. Shibata, H. Kai, T. Ichiki, T. Morisaki, K. Fukuyama, H. Ono, N. Iino, S. Masuda, H. Shimokawa, et al. Apoptosis Induced by Inhibition of Cyclic AMP Response Element-Binding Protein in Vascular Smooth Muscle Cells Circulation, September 9, 2003; 108(10): 1246 - 1252. [Abstract] [Full Text] [PDF]
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 B. S. Buetow, K. A. Tappan, J. R. Crosby, R. A. Seifert, and D. F. Bowen-Pope Chimera Analysis Supports a Predominant Role of PDGFR{beta} in Promoting Smooth-Muscle Cell Chemotaxis after Arterial Injury Am. J. Pathol., September 1, 2003; 163(3): 979 - 984. [Abstract] [Full Text] [PDF]
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M. Sata, K. Tanaka, N. Ishizaka, Y. Hirata, and R. Nagai Absence of p53 Leads to Accelerated Neointimal Hyperplasia After Vascular Injury Arterioscler. Thromb. Vasc. Biol., September 1, 2003; 23(9): 1548 - 1552. [Abstract] [Full Text] [PDF]
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H. Hao, G. Gabbiani, and M.-L. Bochaton-Piallat Arterial Smooth Muscle Cell Heterogeneity: Implications for Atherosclerosis and Restenosis Development Arterioscler. Thromb. Vasc. Biol., September 1, 2003; 23(9): 1510 - 1520. [Abstract] [Full Text] [PDF]
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K.-W. Park, H.-M. Yang, S.-W. Youn, H.-J. Yang, I.-H. Chae, B.-H. Oh, M.-M. Lee, Y.-B. Park, Y.-S. Choi, H.-S. Kim, et al. Constitutively Active Glycogen Synthase Kinase-3{beta} Gene Transfer Sustains Apoptosis, Inhibits Proliferation of Vascular Smooth Muscle Cells, and Reduces Neointima Formation After Balloon Injury in Rats Arterioscler. Thromb. Vasc. Biol., August 1, 2003; 23(8): 1364 - 1369. [Abstract] [Full Text] [PDF]
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D. A. Goukassian, R. Kishore, K. Krasinski, C. Dolan, C. Luedemann, Y.-s. Yoon, M. Kearney, A. Hanley, H. Ma, T. Asahara, et al. Engineering the Response to Vascular Injury: Divergent Effects of Deregulated E2F1 Expression on Vascular Smooth Muscle Cells and Endothelial Cells Result in Endothelial Recovery and Inhibition of Neointimal Growth Circ. Res., July 25, 2003; 93(2): 162 - 169. [Abstract] [Full Text] [PDF]
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E.-L. Marchand, S. Der Sarkissian, P. Hamet, and D. deBlois Caspase-Dependent Cell Death Mediates the Early Phase of Aortic Hypertrophy Regression in Losartan-Treated Spontaneously Hypertensive Rats Circ. Res., April 18, 2003; 92(7): 777 - 784. [Abstract] [Full Text] [PDF]
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R. Kraemer Reduced Apoptosis and Increased Lesion Development in the Flow-Restricted Carotid Artery of p75NTR-Null Mutant Mice Circ. Res., September 20, 2002; 91(6): 494 - 500. [Abstract] [Full Text] [PDF]
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 M. G. Andreassi, N. Botto, A. Rizza, M. G. Colombo, C. Palmieri, S. Berti, S. Manfredi, S. Masetti, A. Clerico, and A. Biagini Deoxyribonucleic acid damage in human lymphocytes after percutaneous transluminal coronary angioplasty J. Am. Coll. Cardiol., September 4, 2002; 40(5): 862 - 868. [Abstract] [Full Text] [PDF]
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E. Durand, Z. Mallat, F. Addad, F. Vilde, M. Desnos, C. Guerot, A. Tedgui, and A. Lafont Time courses of apoptosis and cell proliferation and their relationship to arterial remodeling and restenosis after angioplasty in an atherosclerotic rabbit model J. Am. Coll. Cardiol., May 15, 2002; 39(10): 1680 - 1685. [Abstract] [Full Text] [PDF]
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 M. R Bennett APOPTOSIS IN THE CARDIOVASCULAR SYSTEM Heart, May 1, 2002; 87(5): 480 - 487. [Full Text] [PDF]
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S. Meiners, M. Laule, W. Rother, C. Guenther, I. Prauka, P. Muschick, G. Baumann, P.-M. Kloetzel, and K. Stangl Ubiquitin-Proteasome Pathway as a New Target for the Prevention of Restenosis Circulation, January 29, 2002; 105(4): 483 - 489. [Abstract] [Full Text] [PDF]
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C. Hay, C. Micko, M. F. Prescott, G. Liau, K. Robinson, and H. De Leon Differential Cell Cycle Progression Patterns of Infiltrating Leukocytes and Resident Cells After Balloon Injury of the Rat Carotid Artery Arterioscler. Thromb. Vasc. Biol., December 1, 2001; 21(12): 1948 - 1954. [Abstract] [Full Text] [PDF]
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D. A. Tulis, W. Durante, X. Liu, A. J. Evans, K. J. Peyton, and A. I. Schafer Adenovirus-Mediated Heme Oxygenase-1 Gene Delivery Inhibits Injury-Induced Vascular Neointima Formation Circulation, November 27, 2001; 104(22): 2710 - 2715. [Abstract] [Full Text] [PDF]
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 W. R. P. Agema, J. W. Jukema, S. N. Pimstone, and J. J. P. Kastelein Genetic aspects of restenosis after percutaneous coronary interventions;towards more tailored therapy Eur. Heart J., November 2, 2001; 22(22): 2058 - 2074. [PDF]
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M. Sata, S. Sugiura, M. Yoshizumi, Y. Ouchi, Y. Hirata, and R. Nagai Acute and Chronic Smooth Muscle Cell Apoptosis After Mechanical Vascular Injury Can Occur Independently of the Fas-Death Pathway Arterioscler. Thromb. Vasc. Biol., November 1, 2001; 21(11): 1733 - 1737. [Abstract] [Full Text] [PDF]
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P. Vermeersch, Z. Nong, E. Stabile, O. Varenne, H. Gillijns, M. Pellens, N. Van Pelt, M. Hoylaerts, I. De Scheerder, D. Collen, et al. L-Arginine Administration Reduces Neointima Formation After Stent Injury in Rats by a Nitric Oxide-Mediated Mechanism Arterioscler. Thromb. Vasc. Biol., October 1, 2001; 21(10): 1604 - 1609. [Abstract] [Full Text] [PDF]
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 B. Zhu, G. Zhao, D. P. Witte, D. Y. Hui, and J. A. Fagin Targeted Overexpression of IGF-I in Smooth Muscle Cells of Transgenic Mice Enhances Neointimal Formation through Increased Proliferation and Cell Migration after Intraarterial Injury Endocrinology, August 1, 2001; 142(8): 3598 - 3606. [Abstract] [Full Text] [PDF]
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C. Patterson, G. A. Stouffer, N. Madamanchi, and M. S. Runge New Tricks for Old Dogs : Nonthrombotic Effects of Thrombin in Vessel Wall Biology Circ. Res., May 25, 2001; 88(10): 987 - 997. [Abstract] [Full Text] [PDF]
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M. E. Matsumura, F. Li, L. Berthoux, B. Wei, D. R. Lobe, C. Jeon, and C. A. McNamara Vascular Injury Induces Posttranscriptional Regulation of the Id3 Gene : Cloning of a Novel Id3 Isoform Expressed During Vascular Lesion Formation in Rat and Human Atherosclerosis Arterioscler. Thromb. Vasc. Biol., May 1, 2001; 21(5): 752 - 758. [Abstract] [Full Text] [PDF]
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N. Sudoh, K. Toba, M. Akishita, J. Ako, M. Hashimoto, K. Iijima, S. Kim, Y.-Q. Liang, Y. Ohike, T. Watanabe, et al. Estrogen Prevents Oxidative Stress-Induced Endothelial Cell Apoptosis in Rats Circulation, February 6, 2001; 103(5): 724 - 729. [Abstract] [Full Text] [PDF]
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 A.-P. Gadeau, H. Chaulet, D. Daret, M. Kockx, J.-M. Daniel-Lamazière, and C. Desgranges Time Course of Osteopontin, Osteocalcin, and Osteonectin Accumulation and Calcification After Acute Vessel Wall Injury J. Histochem. Cytochem., January 1, 2001; 49(1): 79 - 86. [Abstract] [Full Text]
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 E. Rodriguez, E. H. Lambert, M. G. Magno, and J. D. Mannion Contractile smooth muscle cell apoptosis early after saphenous vein grafting Ann. Thorac. Surg., October 1, 2000; 70(4): 1145 - 1152. [Abstract] [Full Text] [PDF]
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K. Walsh, R. C. Smith, and H.-S. Kim Vascular Cell Apoptosis in Remodeling, Restenosis, and Plaque Rupture Circ. Res., August 4, 2000; 87(3): 184 - 188. [Full Text] [PDF]
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S. Yasuda, T. Noguchi, M. Gohda, T. Arai, N. Tsutsui, T. Matsuda, and H. Nonogi Single Low-Dose Administration of Human Recombinant Hepatocyte Growth Factor Attenuates Intimal Hyperplasia in a Balloon-Injured Rabbit Iliac Artery Model Circulation, May 30, 2000; 101(21): 2546 - 2549. [Abstract] [Full Text] [PDF]
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G. H. Gibbons and M. J. Pollman Death Receptors, Intimal Disease, and Gene Therapy : Are Therapies That Modify Cell Fate Moving too Fas? Circ. Res., May 26, 2000; 86(10): 1009 - 1012. [Full Text] [PDF]
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H.-S. Kim, K.-K. Hwang, J.-W. Seo, S.-Y. Kim, B.-H. Oh, M.-M. Lee, and Y.-B. Park Apoptosis and Regulation of Bax and Bcl-X Proteins During Human Neonatal Vascular Remodeling Arterioscler. Thromb. Vasc. Biol., April 1, 2000; 20(4): 957 - 963. [Abstract] [Full Text] [PDF]
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 J. Lemay, P. Hamet, and D. deBlois Losartan-induced apoptosis as a novel mechanism for the prevention of vascular lesion formation after injury Journal of Renin-Angiotensin-Aldosterone System, March 1, 2000; 1(1): 46 - 50. [Abstract] [PDF]
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H. Perlman, M. Sata, K. Krasinski, T. Dorai, R. Buttyan, and K. Walsh Adenovirus-encoded hammerhead ribozyme to Bcl-2 inhibits neointimal hyperplasia and induces vascular smooth muscle cell apoptosis Cardiovasc Res, February 1, 2000; 45(3): 570 - 578. [Abstract] [Full Text] [PDF]
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N. J. McCarthy and M. Bennett The regulation of vascular smooth muscle cell apoptosis Cardiovasc Res, February 1, 2000; 45(3): 747 - 755. [Abstract] [Full Text] [PDF]
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K. Walsh and J. M. Isner Apoptosis in inflammatory-fibroproliferative disorders of the vessel wall Cardiovasc Res, February 1, 2000; 45(3): 756 - 765. [Abstract] [Full Text] [PDF]
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A. M. Holm, C. B. Andersen, S. Haunso, and P. Riis Hansen ACE-inhibition promotes apoptosis after balloon injury of rat carotid arteries Cardiovasc Res, February 1, 2000; 45(3): 777 - 782. [Abstract] [Full Text] [PDF]
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C. Mao, O. T.-B. Malek, M. E. Pueyo, P. G. Steg, and F. Soubrier Differential Expression of Rat Frizzled-Related frzb-1 and Frizzled Receptor fz1 and fz2 Genes in the Rat Aorta After Balloon Injury Arterioscler. Thromb. Vasc. Biol., January 1, 2000; 20(1): 43 - 51. [Abstract] [Full Text] [PDF]
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T. Imanishi, J. McBride, Q. Ho, K. D. O’Brien, S. M. Schwartz, and D. K. M. Han Expression of Cellular FLICE-Inhibitory Protein in Human Coronary Arteries and in a Rat Vascular Injury Model Am. J. Pathol., January 1, 2000; 156(1): 125 - 137. [Abstract] [Full Text] [PDF]
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 Y. Ono, H. Ono, H. Matsuoka, T. Fujimori, and E. D. Frohlich Apoptosis, Coronary Arterial Remodeling, and Myocardial Infarction After Nitric Oxide Inhibition in SHR Hypertension, October 1, 1999; 34(4): 609 - 616. [Abstract] [Full Text] [PDF]
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J. Y. Jeremy, D. Rowe, A. M. Emsley, and A. C. Newby Nitric oxide and the proliferation of vascular smooth muscle cells Cardiovasc Res, August 15, 1999; 43(3): 580 - 594. [Full Text] [PDF]
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 G. M. Hirsch, J. Kearsey, T. Burt, M. J. Karnovsky, and T. Lee Medial smooth muscle cell loss in arterial allografts occurs by cytolytic cell induced apoptosis Eur. J. Cardiothorac. Surg., July 1, 1999; 14(1): 89 - 97. [Abstract] [Full Text] [PDF]
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J. D. Smith, S. R. Bryant, L. L. Couper, C. P. H. Vary, P. J. Gotwals, V. E. Koteliansky, and V. Lindner Soluble Transforming Growth Factor-ß Type II Receptor Inhibits Negative Remodeling, Fibroblast Transdifferentiation, and Intimal Lesion Formation But Not Endothelial Growth Circ. Res., May 28, 1999; 84(10): 1212 - 1222. [Abstract] [Full Text] [PDF]
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T. Mano, Z. Luo, S. L. Malendowicz, T. Evans, and K. Walsh Reversal of GATA-6 Downregulation Promotes Smooth Muscle Differentiation and Inhibits Intimal Hyperplasia in Balloon-Injured Rat Carotid Artery Circ. Res., April 2, 1999; 84(6): 647 - 654. [Abstract] [Full Text] [PDF]
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M. R Bennett Apoptosis of vascular smooth muscle cells in vascular remodelling and atherosclerotic plaque rupture Cardiovasc Res, February 1, 1999; 41(2): 361 - 368. [Abstract] [Full Text] [PDF]
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M. J. Pollman, J. L. Hall, and G. H. Gibbons Determinants of Vascular Smooth Muscle Cell Apoptosis After Balloon Angioplasty Injury : Influence of Redox State and Cell Phenotype Circ. Res., January 22, 1999; 84(1): 113 - 121. [Abstract] [Full Text] [PDF]
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 S. K. Sharma, D. Chapman, R. Temsah, T. Netticadan, D. P. Brasil, and N. S. Dhalla Prevention of Vascular Apoptosis in Myocardial Infarction by Losartan Journal of Cardiovascular Pharmacology and Therapeutics, January 1, 1999; 4(2): 77 - 84. [Abstract] [PDF]
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P. J. M. Best, D. Hasdai, G. Sangiorgi, R. S. Schwartz, D. R. Holmes Jr, R. D. Simari, and A. Lerman Apoptosis : Basic Concepts and Implications in Coronary Artery Disease Arterioscler. Thromb. Vasc. Biol., January 1, 1999; 19(1): 14 - 22. [Abstract] [Full Text] [PDF]
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M. M. Kockx Apoptosis in the Atherosclerotic Plaque : Quantitative and Qualitative Aspects Arterioscler. Thromb. Vasc. Biol., October 1, 1998; 18(10): 1519 - 1522. [Abstract] [Full Text] [PDF]
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J. M. Miano, L. A. Kelly, C. A. Artacho, T. A. Nuckolls, R. Piantedosi, and W. S. Blaner all-Trans-Retinoic Acid Reduces Neointimal Formation and Promotes Favorable Geometric Remodeling of the Rat Carotid Artery After Balloon Withdrawal Injury Circulation, September 22, 1998; 98(12): 1219 - 1227. [Abstract] [Full Text] [PDF]
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A. Haunstetter and S. Izumo Apoptosis : Basic Mechanisms and Implications for Cardiovascular Disease Circ. Res., June 15, 1998; 82(11): 1111 - 1129. [Full Text] [PDF]
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S. Kim, Y. Izumi, M. Yano, A. Hamaguchi, K. Miura, S. Yamanaka, H. Miyazaki, and H. Iwao Angiotensin Blockade Inhibits Activation of Mitogen-Activated Protein Kinases in Rat Balloon-Injured Artery Circulation, May 5, 1998; 97(17): 1731 - 1737. [Abstract] [Full Text] [PDF]
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J. E. O'Brien Jr, M. L. Ormont, Y. Shi, D. Wang, A. Zalewski, and J. D. Mannion Early Injury to the Media After Saphenous Vein Grafting Ann. Thorac. Surg., May 1, 1998; 65(5): 1273 - 1278. [Abstract] [Full Text] [PDF]
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H. Wang and J. A. Keiser Molecular characterization of rabbit CPP32 and its function in vascular smooth muscle cell apoptosis Am J Physiol Heart Circ Physiol, April 1, 1998; 274(4): H1132 - H1140. [Abstract] [Full Text] [PDF]
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S. Baek and K. L. March Gene Therapy for Restenosis : Getting Nearer the Heart of the Matter Circ. Res., February 23, 1998; 82(3): 295 - 305. [Abstract] [Full Text] [PDF]
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 M. Sata, H. Perlman, D. A. Muruve, M. Silver, M. Ikebe, T. A. Libermann, P. Oettgen, and K. Walsh Fas ligand gene transfer to the vessel wall inhibits neointima formation and overrides the adenovirus-mediated T cell response PNAS, February 3, 1998; 95(3): 1213 - 1217. [Abstract] [Full Text] [PDF]
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H. Yaoita, K. Ogawa, K. Maehara, and Y. Maruyama Attenuation of Ischemia/Reperfusion Injury in Rats by a Caspase Inhibitor Circulation, January 27, 1998; 97(3): 276 - 281. [Abstract] [Full Text] [PDF]
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E. T.H. Yeh Life and Death in the Cardiovascular System Circulation, February 18, 1997; 95(4): 782 - 786. [Full Text]
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