(Circulation. 2000;101:1362.)
© 2000 American Heart Association, Inc.
Brief Rapid Communications |
Direct In Vivo Evidence Demonstrating Neointimal Migration of Adventitial Fibroblasts After Balloon Injury of Rat Carotid Arteries
From the Departments of Medicine, Vascular Biology and Hypertension Program (G.L., S.-J.C., S.O., Y.F.-C., J.A.T.), and Surgery, Division of Transplantation (J.A.T.), University of Alabama at Birmingham.
Correspondence to John A. Thompson, PhD, 752 Lyons Harrison Research Building, 701 19th Street South, Birmingham, AL 35294-0007. E-mail athompson{at}ms.surgery.uab.edu
Background—Clinical and experimental evidence suggest that the adventitia participates in the response to endoluminal vascular injury. The current study used a direct approach to test the hypothesis that, after balloon injury of the rat carotid artery, adventitial fibroblasts migrate in a luminal direction and contribute to neointima formation.
Methods and Results—Primary syngeneic adventitial fibroblasts were stably transduced with retroviral particles coordinating expression of ß-galactosidase (LacZ) and introduced into the adventitia of right carotid arteries of rats immediately after balloon injury. At defined times after injury and fibroblast implantation, rats were euthanized, and arterial tissue was examined for detection of LacZ mRNA (reverse transcription polymerase chain reaction), DNA (polymerase chain reaction), and in situ enzymatic activity. LacZ expression was detected in the media 5 days postinjury and in both media and neointima at 7, 10, and 14 days postinjury. LacZ was undetectable in injured vessels that had not been seeded with transduced fibroblasts and was restricted to the adventitia in seeded vessels that were not injured.
Conclusions—These observations provide direct demonstration of adventitial fibroblast migration into neointima of arteries after endoluminal injury.
Key Words: adventitial fibroblasts • migration • carotid arteries • vascular injury
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|
|
|
|
|
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|
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|
|
|
|
|
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|
|
|
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|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
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|
|
|
|
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|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
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|
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|
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