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Circulation. 1999;99:2164-2170

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(Circulation. 1999;99:2164-2170.)
© 1999 American Heart Association, Inc.

Basic Science Reports

Inhibition of Intimal Thickening After Balloon Angioplasty in Porcine Coronary Arteries by Targeting Regulators of the Cell Cycle

Richard Gallo, MD; Adrian Padurean, MD; Thottala Jayaraman, PhD; Steven Marx, MD; Merce Roque, MD; Steven Adelman, PhD; James Chesebro, MD; John Fallon, MD; Valentin Fuster, MD, PhD; Andrew Marks, MD, PhD; Juan José Badimon, PhD

From the Cardiovascular Biology Research Laboratory, the Zena and Michael Wiener Cardiovascular Institute (R.G., A.P., M.R., J.C., J.F., V.F., J.J.B.), and the Department of Pathology (J.F.), Mount Sinai School of Medicine, New York, NY; the Molecular Cardiology Program, Columbia University, College of Physicians and Surgeons, New York, NY (T.J., S.M., A.M.); and Wyeth-Ayerst, Princeton, NJ (S.A.).

Correspondence to Juan José Badimon, PhD, Cardiovascular Biology Research Laboratory, Zena and Michael Wiener Cardiovascular Institute, Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, NY-10029. E-mail jjb-laboratory{at}smtplink.mssm.edu

Background—Although percutaneous transluminal coronary angioplasty (PTCA) is a highly effective procedure to reduce the severity of stenotic coronary atherosclerotic disease, its long-term success is significantly limited by the high rate of restenosis. Several cellular and molecular mechanisms have been implicated in the development of restenosis post-PTCA, including vascular smooth muscle cell (VSMC) activation, migration, and proliferation. Recently, our group demonstrated that rapamycin, an immunosuppressant agent with antiproliferative properties, inhibits both rat and human VSMC proliferation and migration in vitro. In the present study, we investigated (1) whether rapamycin administration could reduce neointimal thickening in a porcine model of restenosis post-PTCA and (2) the mechanism by which rapamycin inhibits VSMCs in vivo.

Methods and Results—PTCA was performed on a porcine model at a balloon/vessel ratio of 1.7±0.2. Coronary arteries were analyzed for neointimal formation 4 weeks after PTCA. Intramuscular administration of rapamycin started 3 days before PTCA at a dose of 0.5 mg/kg and continued for 14 days at a dose of 0.25 mg/kg. Cyclin-dependent kinase inhibitor (CDKI) p27kip1 protein levels and pRb phosphorylation within the vessel wall were determined by immunoblot analysis. PTCA in the control group was associated with the development of significant luminal stenosis 4 weeks after the coronary intervention. Luminal narrowing was a consequence of significant neointimal formation in the injured areas. Rapamycin administration was associated with a significant inhibition in coronary stenosis (63±3.4% versus 36±4.5%; P<0.001), resulting in a concomitant increase in luminal area (1.74±0.1 mm2 versus 3.3±0.4 mm2; P<0.001) after PTCA. Inhibition of proliferation was associated with markedly increased concentrations of the p27kip1 levels and inhibition of pRb phosphorylation within the vessel wall.

Conclusions—Rapamycin administration significantly reduced the arterial proliferative response after PTCA in the pig by increasing the level of the CDKI p27kip1 and inhibition of the pRb phosphorylation within the vessel wall. Therefore, pharmacological interventions that elevate CDKI in the vessel wall and target cyclin-dependent kinase activity may have a therapeutic role in the treatment of restenosis after angioplasty in humans.


Key Words: restenosis • cells • angioplasty




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P. S. Brara, M. Moussavian, M. A. Grise, J. P. Reilly, M. Fernandez, R. A. Schatz, and P. S. Teirstein
Pilot Trial of Oral Rapamycin for Recalcitrant Restenosis
Circulation, April 8, 2003; 107(13): 1722 - 1724.
[Abstract] [Full Text] [PDF]

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 Nephrol Dial TransplantHome page
R. de Graaf, R. Dammers, T. Vainas, A. P. G. Hoeks, and J. H. M. Tordoir
Detection of cell-cycle regulators in failed arteriovenous fistulas for haemodialysis
Nephrol. Dial. Transplant., April 1, 2003; 18(4): 814 - 818.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
A. Diez-Juan and V. Andres
Coordinate Control of Proliferation and Migration by the p27Kip1/Cyclin-Dependent Kinase/Retinoblastoma Pathway in Vascular Smooth Muscle Cells and Fibroblasts
Circ. Res., March 7, 2003; 92(4): 402 - 410.
[Abstract] [Full Text] [PDF]

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 HeartHome page
M. R Bennett
IN-STENT STENOSIS: PATHOLOGY AND IMPLICATIONS FOR THE DEVELOPMENT OF DRUG ELUTING STENTS
Heart, February 1, 2003; 89(2): 218 - 224.
[Full Text] [PDF]

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 CirculationHome page
D. A. Tulis, Z. H. Mnjoyan, R. L. Schiesser, H. S. Shelat, A. J. Evans, P. Zoldhelyi, and K. Fujise
Adenoviral Gene Transfer of Fortilin Attenuates Neointima Formation Through Suppression of Vascular Smooth Muscle Cell Proliferation and Migration
Circulation, January 7, 2003; 107(1): 98 - 105.
[Abstract] [Full Text] [PDF]

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 Physiol. GenomicsHome page
T. H. Kim, K. A. Skelding, E. G. Nabel, and R. D. Simari
What can cardiovascular gene transfer learn from genomics: and vice versa?
Physiol Genomics, December 3, 2002; 11(3): 179 - 182.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
M. N. Babapulle and M. J. Eisenberg
Coated Stents for the Prevention of Restenosis: Part I
Circulation, November 19, 2002; 106(21): 2734 - 2740.
[Full Text] [PDF]

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 CirculationHome page
A. Farb, M. John, E. Acampado, F. D. Kolodgie, M. F. Prescott, and R. Virmani
Oral Everolimus Inhibits In-Stent Neointimal Growth
Circulation, October 29, 2002; 106(18): 2379 - 2384.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
S. H. Duda, B. Pusich, G. Richter, P. Landwehr, V. L. Oliva, A. Tielbeek, B. Wiesinger, J. B. Hak, H. Tielemans, G. Ziemer, et al.
Sirolimus-Eluting Stents for the Treatment of Obstructive Superficial Femoral Artery Disease: Six-Month Results
Circulation, September 17, 2002; 106(12): 1505 - 1509.
[Abstract] [Full Text] [PDF]

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 Eur Heart J SupplHome page
V. Fuster, R. Corti, Z.A. Fayad, and J.J. Badimon
Understanding the pathophysiology of the arterial wall: which method should we choose? Magnetic resonance imaging
Eur. Heart J. Suppl., September 1, 2002; 4(suppl_F): F41 - F46.
[Abstract] [PDF]

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 J. Lipid Res.Home page
J. D. Morrisett, G. Abdel-Fattah, R. Hoogeveen, E. Mitchell, C. M. Ballantyne, H. J. Pownall, A. R. Opekun, J. S. Jaffe, S. Oppermann, and B. D. Kahan
Effects of sirolimus on plasma lipids, lipoprotein levels, and fatty acid metabolism in renal transplant patients
J. Lipid Res., August 1, 2002; 43(8): 1170 - 1180.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
M.-C. Morice, P. W. Serruys, J. E. Sousa, J. Fajadet, E. Ban Hayashi, M. Perin, A. Colombo, G. Schuler, P. Barragan, G. Guagliumi, et al.
A Randomized Comparison of a Sirolimus-Eluting Stent with a Standard Stent for Coronary Revascularization
N. Engl. J. Med., June 6, 2002; 346(23): 1773 - 1780.
[Abstract] [Full Text] [PDF]

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 HeartHome page
P W Serruys, E Regar, and A J Carter
Rapamycin eluting stent: the onset of a new era in interventional cardiology
Heart, April 1, 2002; 87(4): 305 - 307.
[Full Text] [PDF]

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 J Am Coll CardiolHome page
H. C. Lowe, S. N. Oesterle, and L. M. Khachigian
Coronary in-stent restenosis: Current status and future strategies
J. Am. Coll. Cardiol., January 16, 2002; 39(2): 183 - 193.
[Abstract] [Full Text] [PDF]

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 Eur Heart JHome page
R. Beyar and A. Roguin
The sirolimus coated stent: will the Achilles heel of interventional cardiology finally be cured?
Eur. Heart J., November 2, 2001; 22(22): 2054 - 2057.
[PDF]

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 Eur Heart JHome page
B.J Rensing, J Vos, P.C Smits, D.P Foley, M.J.B.M van den Brand, W.J van der Giessen, P.J de Feijter, and P.W Serruys
Coronary restenosis elimination with a sirolimus eluting stent; First European human experience with 6-month angiographic and intravascular ultrasonic follow-up
Eur. Heart J., November 2, 2001; 22(22): 2125 - 2130.
[Abstract] [PDF]

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 CirculationHome page
P. S. Teirstein
Living the Dream of No Restenosis
Circulation, October 23, 2001; 104(17): 1996 - 1998.
[Full Text] [PDF]

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 CirculationHome page
J. E. Sousa, M. A. Costa, A. C. Abizaid, B. J. Rensing, A. S. Abizaid, L. F. Tanajura, K. Kozuma, G. Van Langenhove, A. G.M.R. Sousa, R. Falotico, et al.
Sustained Suppression of Neointimal Proliferation by Sirolimus-Eluting Stents: One-Year Angiographic and Intravascular Ultrasound Follow-Up
Circulation, October 23, 2001; 104(17): 2007 - 2011.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
T. Suzuki, G. Kopia, S.-i. Hayashi, L. R. Bailey, G. Llanos, R. Wilensky, B. D. Klugherz, G. Papandreou, P. Narayan, M. B. Leon, et al.
Stent-Based Delivery of Sirolimus Reduces Neointimal Formation in a Porcine Coronary Model
Circulation, September 4, 2001; 104(10): 1188 - 1193.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
A. DIEZ-JUAN and V. ANDRES
The growth suppressor p27Kip1 protects against diet-induced atherosclerosis
FASEB J, September 1, 2001; 15(11): 1989 - 1995.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
S. O. Marx and A. R. Marks
Bench to Bedside: The Development of Rapamycin and Its Application to Stent Restenosis
Circulation, August 21, 2001; 104(8): 852 - 855.
[Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
R. C. Braun-Dullaeus, M. J. Mann, U. Seay, L. Zhang, H. E. von der Leyen, R. E. Morris, and V. J. Dzau
Cell Cycle Protein Expression in Vascular Smooth Muscle Cells In Vitro and In Vivo Is Regulated Through Phosphatidylinositol 3-Kinase and Mammalian Target of Rapamycin
Arterioscler Thromb Vasc Biol, July 1, 2001; 21(7): 1152 - 1158.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
M. Boehm and E. G. Nabel
Cell Cycle and Cell Migration : New Pieces to the Puzzle
Circulation, June 19, 2001; 103(24): 2879 - 2881.
[Full Text] [PDF]

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 CirculationHome page
J. Sun, S. O. Marx, H.-J. Chen, M. Poon, A. R. Marks, and L. E. Rabbani
Role for p27Kip1 in Vascular Smooth Muscle Cell Migration
Circulation, June 19, 2001; 103(24): 2967 - 2972.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
V. Sriram and C. Patterson
Cell Cycle in Vasculoproliferative Diseases : Potential Interventions and Routes of Delivery
Circulation, May 15, 2001; 103(19): 2414 - 2419.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
S. Wakino, U. Kintscher, S. Kim, S. Jackson, F. Yin, S. Nagpal, R. A. S. Chandraratna, W. A. Hsueh, and R. E. Law
Retinoids Inhibit Proliferation of Human Coronary Smooth Muscle Cells by Modulating Cell Cycle Regulators
Arterioscler Thromb Vasc Biol, May 1, 2001; 21(5): 746 - 751.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
D. Zohlnhofer, C. A. Klein, T. Richter, R. Brandl, A. Murr, T. Nuhrenberg, A. Schomig, P. A. Baeuerle, and F.-J. Neumann
Gene Expression Profiling of Human Stent-Induced Neointima by cDNA Array Analysis of Microscopic Specimens Retrieved by Helix Cutter Atherectomy : Detection of FK506-Binding Protein 12 Upregulation
Circulation, March 13, 2001; 103(10): 1396 - 1402.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
T. NISHIMURA, J. L. FAUL, G. J. BERRY, I. VEVE, R. G. PEARL, and P. N. KAO
40-O-(2-Hydroxyethyl)-rapamycin Attenuates Pulmonary Arterial Hypertension and Neointimal Formation in Rats
Am. J. Respir. Crit. Care Med., February 1, 2001; 163(2): 498 - 502.
[Abstract] [Full Text]

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 CirculationHome page
J. E. Sousa, M. A. Costa, A. Abizaid, A. S. Abizaid, F. Feres, I. M. F. Pinto, A. C. Seixas, R. Staico, L. A. Mattos, A. G. M. R. Sousa, et al.
Lack of Neointimal Proliferation After Implantation of Sirolimus-Coated Stents in Human Coronary Arteries : A Quantitative Coronary Angiography and Three-Dimensional Intravascular Ultrasound Study
Circulation, January 16, 2001; 103(2): 192 - 195.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
M. Kawauchi, J.-i. Suzuki, R. Morishita, Y. Wada, A. Izawa, N. Tomita, J. Amano, Y. Kaneda, T. Ogihara, S. Takamoto, et al.
Gene Therapy for Attenuating Cardiac Allograft Arteriopathy Using Ex Vivo E2F Decoy Transfection by HVJ-AVE-Liposome Method in Mice and Nonhuman Primates
Circ. Res., November 24, 2000; 87(11): 1063 - 1068.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
F. D. Kolodgie, A. Farb, and R. Virmani
Local Delivery of Ceramide for Restenosis : Is There a Future for Lipid Therapy?
Circ. Res., August 18, 2000; 87(4): 264 - 267.
[Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
U. Kintscher, S. Wakino, S. Kim, S. M. Jackson, E. Fleck, W. A. Hsueh, and R. E. Law
Doxazosin Inhibits Retinoblastoma Protein Phosphorylation and G1->S Transition in Human Coronary Smooth Muscle Cells
Arterioscler Thromb Vasc Biol, May 1, 2000; 20(5): 1216 - 1224.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
F. Peiretti, S. Lopez, P. Deprez-Beauclair, B. Bonardo, I. Juhan-Vague, and G. Nalbone
Inhibition of p70S6 Kinase during Transforming Growth Factor-beta 1/Vitamin D3-induced Monocyte Differentiation of HL-60 Cells Allows Tumor Necrosis Factor-alpha to Stimulate Plasminogen Activator Inhibitor-1 Synthesis
J. Biol. Chem., August 17, 2001; 276(34): 32214 - 32219.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. Zhao, J. Letterman, and B. M. Schreiber
beta -Migrating Very Low Density Lipoprotein (beta VLDL) Activates Smooth Muscle Cell Mitogen-activated Protein (MAP) Kinase via G Protein-coupled Receptor-mediated Transactivation of the Epidermal Growth Factor (EGF) Receptor. EFFECT OF MAP KINASE ACTIVATION ON beta VLDL PLUS EGF-INDUCED CELL PROLIFERATION
J. Biol. Chem., August 10, 2001; 276(33): 30579 - 30588.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
T. S. Mahoney, A. S. Weyrich, D. A. Dixon, T. McIntyre, S. M. Prescott, and G. A. Zimmerman
Cell adhesion regulates gene expression at translational checkpoints in human myeloid leukocytes
PNAS, August 28, 2001; 98(18): 10284 - 10289.
[Abstract] [Full Text] [PDF]


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