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(Circulation. 2000;101:235.)
© 2000 American Heart Association, Inc.
Brief Rapid Communications |
Modulation of Vascular Inflammation In Vitro and In Vivo by Peroxisome Proliferator–Activated Receptor-
Activators
From the Department of Internal Medicine (V.P., H.D.W., J.T.W., E.T.H.Y.) and Institute of Molecular Medicine for the Prevention of Human Diseases (E.T.H.Y.), University of Texas Health Science Center, and Texas Heart Institute (V.P., J.T.W., E.T.H.Y.), St Luke’s Episcopal Hospital, Houston.
Correspondence to Edward T.H. Yeh, MD, Department of Internal Medicine, 6431 Fannin, Suite 4200, UT-Houston HSC, Houston, TX 77030.
 |
Abstract |
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 Top Abstract IntroductionMethodsResultsDiscussionReferences |
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Background—Peroxisome proliferator–activated receptor-
(PPAR) is expressed in
atherosclerotic plaques and in endothelial cells. The
possible effects of PPAR activators on
endothelial activation and inflammatory response within
the plaque are currently unknown.
Methods and Results—We tested the hypothesis that PPAR
activators inhibit vascular cell adhesion molecule (VCAM-1)
and intercellular adhesion molecule (ICAM-1) expression in cultured
endothelial cells (evaluated by flow cytometry) and
homing of monocyte/macrophages to atherosclerotic plaques in
vivo. In endothelial cells, the PPAR agonists
troglitazone at 100 µmol/L and
15-deoxy-
12,14-prostaglandin
J2 (15d-PGJ2) at 20 µmol/L markedly attenuated the
tumor necrosis factor–induced expression of VCAM-1 and ICAM-1. A
significant inhibition of VCAM-1 expression was also evident at 5 and
10 µmol/L 15d-PGJ2 and 20 µmol/L troglitazone. Expression
of E-selectin and PECAM-1 was not altered. To confirm the biological
relevance of these results, we assessed the effects of troglitazone on
monocyte/macrophage homing to atherosclerotic plaques in
apoE-deficient mice. A 7-day treatment with troglitazone (400 mg/kg)
significantly reduced monocyte/macrophage homing to
atherosclerotic plaques (236±77 versus 177±43 macrophages,
P=0.03); an even more striking inhibition was found at
3200 mg/kg troglitazone (344±76 versus 172±83 macrophages,
P=0.005).
Conclusions—PPAR activators inhibit expression of
VCAM-1 and ICAM-1 in activated endothelial
cells and significantly reduce monocyte/macrophage homing to
atherosclerotic plaques. These findings suggest that PPAR
activators, currently used in treatment of type II
diabetes, may have beneficial effects in modulating inflammatory
response in atherosclerosis.
Key Words: cell adhesion molecules • receptors • atherosclerosis
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Introduction |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Experimental and pathological studies have suggested that the peroxisome proliferator–activated receptor-
(PPAR)
may have a role in the pathogenesis of
atherosclerosis.1 PPAR is a nuclear
receptor highly expressed in several tissues, including adipose tissue,
monocytes/macrophages, and smooth muscle cells.2
In atherosclerotic plaques, PPAR is expressed by
macrophage/foam cells, and activation of this receptor can
inhibit macrophage activation.3 4 Although PPAR
is also expressed by endothelial cells,5
the possible effects of PPAR activators in
atherosclerotic plaques are currently unknown.
Expression of adhesion molecules by endothelial cells
and adhesion of leukocytes to endothelial cells is an
essential step in atherogenesis.6 7 We have recently
shown, in an animal model of atherosclerosis, that
monocyte/macrophage homing to atherosclerotic plaques depends
on the expression of the adhesion molecules vascular cell adhesion
molecule (VCAM-1) and intercellular adhesion molecule
(ICAM-1).8 The aim of our study was to assess the effects
of PPAR activators on the expression of adhesion
molecules on activated endothelial cells and on
monocyte/macrophage homing to atherosclerotic plaques in
vivo.
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Methods |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Cell Cultures
Human umbilical vein endothelial cells (HUVECs, Cascade Biology) were grown in M199 medium with 15% FBS, 0.2 mg/mL heparin, 0.1 mg/mL endothelial cell growth supplement (Biomedical Technologies), 2 mmol/L L-glutamine, and 1% penicillin/streptomycin. Cells were used at passage 2 to 4. Viability by trypan blue exclusion was >95% in each experiment. Apoptosis was assessed by detection of fragmented DNA at flow cytometry after staining with propidium iodide, according to a previously published protocol.9
Mouse RAW 264.7 cells were grown in DMEM with 10% FBS, 2 mmol/L L-glutamine, and 1% penicillin/streptomycin.
Detection of Adhesion Molecules
HUVECs were pretreated with the PPAR agonists troglitazone
(Parke-Davis), ciglitazone (Biomol),
15-deoxy-12,14-prostaglandin
J2 (15d-PGJ2, from Calbiochem); with the PPAR
agonist fenofibrate (Sigma); or with vehicle (0.1% DMSO) at the
concentrations indicated. After 2 hours, the cells were incubated with
tumor necrosis factor (TNF)- at 10 ng/mL for 12 hours. Cells were
detached with 10 mmol/L EDTA in PBS (without trypsin) and stained
with R-phycoerythrin–labeled monoclonal antibodies
(Pharmingen) against VCAM-1 (CD106), ICAM-1 (CD54), or PECAM-1 (CD31)
with FITC-labeled monoclonal antibodies (R and D)
against E-selectin (CD62E) or with the appropriate isotype IgG
(phycoerythrin or FITC) as control. Fluorescence
intensity of 9000 cells for each sample was quantified by a
FACSCalibur analyzer (Becton-Dickinson). All experiments
were performed in triplicate.
Monocyte/Macrophage Homing to Atherosclerotic
Plaques
Monocyte/macrophage homing to the atherosclerotic
plaques in vivo was assessed according to a previously published
protocol,8 modified to use a RAW murine macrophage
cell line rather than activated peritoneal macrophages.
RAW 267.4 cells were incubated for 75 minutes with 2-µm
fluorescent microspheres (Molecular Probes). Cells were
then injected into the tail vein of apoE knockout mice
(10x106 cells per mouse).8 The mice
were euthanized after 48 hours. Labeled cells adhering to or
present inside the atheromatous plaque were
quantified in 200 serial sections covering the first 1 mm of the
ascending aorta. To validate RAW cells as monocyte/macrophage
surrogates in our animal model, we performed an inhibition experiment
by pretreating apoE-deficient mice with monoclonal antibody against
integrin-4 (R1-2, from Pharmingen) 6 hours before injection with RAW
cells.
Mice (6 to 8 in each group) were randomized to troglitazone administered by gavage (0.5-mL suspension in water 2 times per day) or to vehicle for 7 days before monocyte/macrophage injection and for the following 2 days. Two different doses of troglitazone (400 mg · kg-1 · d-1 or 3200 mg · kg-1 · d-1) were tested in 2 studies.
Statistics
Results are expressed as mean±SD. Monocyte/macrophage
homing was analyzed with the Mann-Whitney U test to
take into account the small sample size. A value of P<0.05
(2-tailed) was considered significant.
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Results |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Expression of Adhesion Molecules
HUVECs showed expression of PECAM-1, low expression of ICAM-1, and no detectable VCAM-1 or E-selectin (Figure 1
). Treatment with 100 µmol/L of
either troglitazone or ciglitazone and 20 µmol/L of 15d-PGJ2 did
not induce apoptosis (apoptotic cells <2% in any
condition) and did not change baseline expression of adhesion molecules
(data not shown). As shown in Figure 1, incubation with TNF-
10 ng/mL for 12 hours significantly increased the expression of ICAM-1
(A and B), VCAM-1 (C and D), and E-selectin (E and F), with no change
in the expression of PECAM-1 (G and H). Pretreatment with troglitazone
at 100 µmol/L and with 15d-PGJ2 20 µmol/L decreased the
expression of both ICAM-1 (A and B) and VCAM-1 (C and D) almost to
baseline levels. In addition, ciglitazone 100 µmol/L (L)
decreased expression of VCAM-1 (but not ICAM-1), with an even stronger
effect at 200 µmol/L (M). A significant reduction of VCAM-1
expression was also evident with 20 µmol/L of troglitazone (O)
and with 5 or 10 µmol/L of 15d-PGJ2 (P and Q), although these
doses did not significantly change expression of ICAM-1 (data not
shown). Expression of E-selectin (E and F) or PECAM-1 (G and H) was not
changed.
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The PPAR agonist fenofibrate at 100 µmol/L was associated
with a slight reduction of VCAM-1 expression after TNF- stimulation
(J) but did not change the expression of ICAM-1 (I) or E-selectin (data
not shown). Other prostaglandins
(PGE2 20 µmol/L and
PGF2 20 µmol/L) did not change
expression of adhesion molecules (data not shown).
Monocyte/Macrophage Homing
Labeled RAW cells migrated to atherosclerotic plaque, and
anti-4 antibodies markedly inhibited this phenomenon (Figure 2). Pretreatment with troglitazone at 400
mg · kg-1 ·
d-1 for 7 days reduced homing of labeled
monocyte/macrophages to atherosclerotic plaques in the aortic
root significantly, by 25% (P=0.03, Figure 2).
High-dose troglitazone (3200 mg ·
kg-1 · d-1) was
associated with a 50% reduction of monocyte/macrophage homing
(P=0.005). Troglitazone treatment did not change serum
levels of total cholesterol, triglycerides, or
glucose.
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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The present study shows that PPAR
activators
markedly decrease expression of adhesion molecules in activated
human endothelial cells. Short-term treatment with the
PPAR activator troglitazone also significantly inhibits
macrophage homing to atherosclerotic plaques.
PPAR is expressed in atherosclerotic plaques, and activation of
PPAR inhibits macrophage activation.3 4 The
antidiabetic drugs thiazolidinediones are specific
activators of PPAR, whereas the natural agonists are
still largely unknown. However, natural polyunsaturated fatty acids can
activate PPAR, and 15d-PGJ2 is the most specific
(KD=2.5
µmol/L).10
PPAR is expressed by human endothelial cells,
including HUVECs.5 Activation of this receptor can inhibit
endothelial cell proliferation and may modulate PAI-1
expression,5 11 reduce endothelin-1
production,12 and induce
apoptosis,13 in particular in serum-free
conditions. Activation of PPAR results in inhibition of the AP-1 and
NF-
B pathways3 12 that regulate the expression of
adhesion molecules by activated endothelial
cells. We found that several PPAR activators inhibit
expression of ICAM-1 and VCAM-1 in activated HUVECs. However,
as in several previous studies,3 4 the response to
troglitazone and ciglitazone occurred at concentrations higher than
their binding affinity for PPAR, whereas the effects of 15d-PGJ2
were in a concentration range compatible with its
KD. The reasons for this discrepancy are
unclear, and activation of additional pathways cannot be excluded.
However, in a recent study using endothelial cells in
conditions similar to our experiments (with complete medium including
serum), only high concentrations (100 µmol/L) of ciglitazone
could activate a PPAR reporter.13 Thus, it
appears that high concentrations of thiazolidinediones are necessary to
activate the PPAR receptor in our experimental
conditions.
Although high concentrations of troglitazone and 15d-PGJ2 (but not of
ciglitazone) may also activate PPAR, this is unlikely to
explain our results, because 5 µmol/L 15d-PGJ2 and 100
µmol/L ciglitazone are not associated with any PPAR
activation.14
Marx et al15 recently reported that PPAR
activators reduced expression of VCAM-1 (but not ICAM-1 and
E-selectin) by activated human saphenous vein
endothelial cells.15 The same study did
not find any significant effect of PPAR agonists (troglitazone or
15d-PGJ2 10 µmol/L) on the expression of adhesion molecules.
Differences in the study design (2-hour pretreatment in our study
versus 24-hour) may explain their negative results, because we found
that inhibition of VCAM-1 expression by PPAR agonists was much less
evident with 24-hour pretreatment than with a 2-hour pretreatment (data
not shown).
We reported previously that in apoE-deficient mice, homing of
activated peritoneal macrophages to atherosclerotic
plaques is reduced by pretreatment with monoclonal antibodies against
ICAM-1 and 4 integrin (the natural ligand for VCAM-1).8
We modified this model to use a mouse macrophage cell line (RAW
267.4) that does not express significant levels of
PPAR.3 Troglitazone treatment significantly inhibits
monocyte/macrophage homing, with a 50% reduction at the
highest dose. However, 400 mg · kg-1
· d-1 of troglitazone, a dose used in mouse
models of diabetes,16 is also associated with a
significant reduction in monocyte/macrophage accumulation.
Similarly, troglitazone inhibits neointimal hyperplasia in
rats.17 Troglitazone also has antioxidant effects, and the
beneficial effects observed in our experiments may not be due only to
PPAR activation.
PPAR activators are used in treatment of type II
diabetes, and in a preliminary study, treatment with troglitazone was
found to reduce carotid intimal-medial thickness, a marker of early
stages of atherosclerosis.18 However,
atherosclerosis is a composite phenomenon involving
many different molecular pathways, and further studies are needed to
assess the effects of PPAR activators on the progression
of atherosclerosis.
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Footnotes |
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Guest editor for this article was Prediman K. Shah, MD, Cedars-Sinai Medical Center, Los Angeles, Calif.
Received September 16, 1999; revision received November 15, 1999; accepted November 18, 1999.
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M.R. Langenfeld, T. Forst, C. Hohberg, P. Kann, G. Lubben, T. Konrad, S.D. Fullert, C. Sachara, and A. Pfutzner Pioglitazone Decreases Carotid Intima-Media Thickness Independently of Glycemic Control in Patients With Type 2 Diabetes Mellitus: Results From a Controlled Randomized Study Circulation, May 17, 2005; 111(19): 2525 - 2531. [Abstract] [Full Text] [PDF]
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 B. Cariou, J.-C. Fruchart, and B. Staels Review: Vascular protective effects of peroxisome proliferator-activated receptor agonists The British Journal of Diabetes & Vascular Disease, May 1, 2005; 5(3): 126 - 132. [Abstract] [PDF]
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M. S. Goligorsky Endothelial cell dysfunction: can't live with it, how to live without it Am J Physiol Renal Physiol, May 1, 2005; 288(5): F871 - F880. [Abstract] [Full Text] [PDF]
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 D. C. W. Lau, B. Dhillon, H. Yan, P. E. Szmitko, and S. Verma Adipokines: molecular links between obesity and atheroslcerosis Am J Physiol Heart Circ Physiol, May 1, 2005; 288(5): H2031 - H2041. [Abstract] [Full Text] [PDF]
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H. Migita and J. Morser 15-Deoxy-{Delta}12,14-Prostaglandin J2 (15d-PGJ2) Signals Through Retinoic Acid Receptor-Related Orphan Receptor-{alpha} but Not Peroxisome Proliferator-Activated Receptor-{gamma} in Human Vascular Endothelial Cells: The Effect of 15d-PGJ2 on Tumor Necrosis Factor-{alpha}-Induced Gene Expression Arterioscler Thromb Vasc Biol, April 1, 2005; 25(4): 710 - 716. [Abstract] [Full Text] [PDF]
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E. L. Schiffrin Peroxisome proliferator-activated receptors and cardiovascular remodeling Am J Physiol Heart Circ Physiol, March 1, 2005; 288(3): H1037 - H1043. [Abstract] [Full Text] [PDF]
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J. W Chu, F. Abbasi, C. Lamendola, T. McLaughlin, G. M Reaven, and P. S Tsao Effect of rosiglitazone treatment on circulating vascular and inflammatory markers in insulin-resistant subjects Diabetes and Vascular Disease Research, February 1, 2005; 2(1): 37 - 41. [Abstract] [PDF]
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 L. Serghides and K. C. Kain Peroxisome Proliferator-Activated Receptor {gamma} and Retinoid X Receptor Agonists Have Minimal Effects on the Interaction of Endothelial Cells with Plasmodium falciparum- Infected Erythrocytes Infect. Immun., February 1, 2005; 73(2): 1209 - 1213. [Abstract] [Full Text] [PDF]
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 J. L. Olivares, M. Vazquez, G. Rodriguez, P. Samper, and J. Fleta Electrocardiographic and Echocardiographic Findings in Malnourished Children J. Am. Coll. Nutr., February 1, 2005; 24(1): 38 - 43. [Abstract] [Full Text] [PDF]
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M. B. Crosby, J. L. Svenson, J. Zhang, C. J. Nicol, F. J. Gonzalez, and G. S. Gilkeson Peroxisome Proliferation-Activated Receptor (PPAR){gamma} Is Not Necessary for Synthetic PPAR{gamma} Agonist Inhibition of Inducible Nitric-Oxide Synthase and Nitric Oxide J. Pharmacol. Exp. Ther., January 1, 2005; 312(1): 69 - 76. [Abstract] [Full Text] [PDF]
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K. M. Park, J. I. Kim, Y. Ahn, A. J. Bonventre, and J. V. Bonventre Testosterone Is Responsible for Enhanced Susceptibility of Males to Ischemic Renal Injury J. Biol. Chem., December 10, 2004; 279(50): 52282 - 52292. [Abstract] [Full Text] [PDF]
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A. S.F. Doney, B. Fischer, G. Leese, A. D. Morris, and C. N.A. Palmer Cardiovascular Risk in Type 2 Diabetes Is Associated With Variation at the PPARG Locus: A Go-DARTS Study Arterioscler Thromb Vasc Biol, December 1, 2004; 24(12): 2403 - 2407. [Abstract] [Full Text] [PDF]
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W. Verreth, D. De Keyzer, M. Pelat, P. Verhamme, J. Ganame, J. K. Bielicki, A. Mertens, R. Quarck, N. Benhabiles, G. Marguerie, et al. Weight Loss-Associated Induction of Peroxisome Proliferator-Activated Receptor-{alpha} and Peroxisome Proliferator-Activated Receptor-{gamma} Correlate With Reduced Atherosclerosis and Improved Cardiovascular Function in Obese Insulin-Resistant Mice Circulation, November 16, 2004; 110(20): 3259 - 3269. [Abstract] [Full Text] [PDF]
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D. Walcher and N. Marx Insulin resistance and cardiovascular disease: the role of PPAR{gamma} activators beyond their anti-diabetic action Diabetes and Vascular Disease Research, October 1, 2004; 1(2): 76 - 81. [Abstract] [PDF]
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 M. Akaike, W. Che, N.-L. Marmarosh, S. Ohta, M. Osawa, B. Ding, B. C. Berk, C. Yan, and J.-i. Abe The Hinge-Helix 1 Region of Peroxisome Proliferator-Activated Receptor {gamma}1 (PPAR{gamma}1) Mediates Interaction with Extracellular Signal-Regulated Kinase 5 and PPAR{gamma}1 Transcriptional Activation: Involvement in Flow-Induced PPAR{gamma} Activation in Endothelial Cells Mol. Cell. Biol., October 1, 2004; 24(19): 8691 - 8704. [Abstract] [Full Text] [PDF]
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 H. S. Lim, R. J. MacFadyen, and G. Y. H. Lip Diabetes Mellitus, the Renin-Angiotensin-Aldosterone System, and the Heart Arch Intern Med, September 13, 2004; 164(16): 1737 - 1748. [Abstract] [Full Text] [PDF]
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Y. Liu, Y. Zhu, F. Rannou, T.-S. Lee, K. Formentin, L. Zeng, X. Yuan, N. Wang, S. Chien, B. M. Forman, et al. Laminar Flow Activates Peroxisome Proliferator-Activated Receptor-{gamma} in Vascular Endothelial Cells Circulation, August 31, 2004; 110(9): 1128 - 1133. [Abstract] [Full Text] [PDF]
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E. Verrier, L. Wang, C. Wadham, N. Albanese, C. Hahn, J. R. Gamble, V. K. K. Chatterjee, M. A. Vadas, and P. Xia PPAR{gamma} Agonists Ameliorate Endothelial Cell Activation via Inhibition of Diacylglycerol-Protein Kinase C Signaling Pathway: Role of Diacylglycerol Kinase Circ. Res., June 11, 2004; 94(11): 1515 - 1522. [Abstract] [Full Text] [PDF]
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J. T. Willerson and P. M. Ridker Inflammation as a Cardiovascular Risk Factor Circulation, June 1, 2004; 109(21_suppl_1): II-2 - II-10. [Abstract] [Full Text] [PDF]
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N. Marx, H. Duez, J.-C. Fruchart, and B. Staels Peroxisome Proliferator-Activated Receptors and Atherogenesis: Regulators of Gene Expression in Vascular Cells Circ. Res., May 14, 2004; 94(9): 1168 - 1178. [Abstract] [Full Text] [PDF]
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J. P.H. van Wijk and T. J. Rabelink PPAR-{gamma} Agonists: Shifting Attention from the Belly to the Heart? Arterioscler Thromb Vasc Biol, May 1, 2004; 24(5): 798 - 800. [Full Text]
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C.-H. Wang, N. Ciliberti, S.-H. Li, P. E. Szmitko, R. D. Weisel, P. W.M. Fedak, M. Al-Omran, W.-J. Cherng, R.-K. Li, W. L. Stanford, et al. Rosiglitazone Facilitates Angiogenic Progenitor Cell Differentiation Toward Endothelial Lineage: A New Paradigm in Glitazone Pleiotropy Circulation, March 23, 2004; 109(11): 1392 - 1400. [Abstract] [Full Text] [PDF]
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P. K. Chatterjee, N. S.A Patel, S. Cuzzocrea, P. A.J Brown, K. N Stewart, H. Mota-Filipe, D. Britti, W. Eberhardt, J. Pfeilschifter, and C. Thiemermann The cyclopentenone prostaglandin 15-deoxy-{Delta}12,14-prostaglandin J2 ameliorates ischemic acute renal failure Cardiovasc Res, February 15, 2004; 61(3): 630 - 643. [Abstract] [Full Text] [PDF]
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 R. Corti, J. I. Osende, J. T. Fallon, V. Fuster, G. Mizsei, H. Jneid, S. D. Wright, W. F. Chaplin, and J. J. Badimon The selective peroxisomal proliferator-activated receptor-gamma agonist has an additive effect on plaque regression in combination with simvastatin in experimental atherosclerosis: in vivo study by high-resolution magnetic resonance imaging J. Am. Coll. Cardiol., February 4, 2004; 43(3): 464 - 473. [Abstract] [Full Text] [PDF]
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L. Tao, H.-R. Liu, E. Gao, Z.-P. Teng, B. L. Lopez, T. A. Christopher, X.-L. Ma, I. Batinic-Haberle, R. N. Willette, E. H. Ohlstein, et al. Antioxidative, Antinitrative, and Vasculoprotective Effects of a Peroxisome Proliferator-Activated Receptor-{gamma} Agonist in Hypercholesterolemia Circulation, December 2, 2003; 108(22): 2805 - 2811. [Abstract] [Full Text] [PDF]
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 C. V. Desouza, S. N. Murthy, J. Diez, B. Dunne, A. S. Matta, V. A. Fonseca, and D. B. McNamara Differential Effects of Peroxisome Proliferator Activator Receptor-{alpha} and {gamma} Ligands on Intimal Hyperplasia After Balloon Catheter-Induced Vascular Injury in Zucker Rats Journal of Cardiovascular Pharmacology and Therapeutics, December 1, 2003; 8(4): 297 - 305. [Abstract] [PDF]
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J. S. Sidhu, D. Cowan, and J.-C. Kaski The effects of rosiglitazone, a peroxisome proliferator-activated receptor-gamma agonist, on markers of endothelial cell activation, C-reactive protein, and fibrinogen levels in non-diabetic coronary artery disease patients J. Am. Coll. Cardiol., November 19, 2003; 42(10): 1757 - 1763. [Abstract] [Full Text] [PDF]
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 E. L. Schiffrin, F. Amiri, K. Benkirane, M. Iglarz, and Q. N. Diep Peroxisome Proliferator-Activated Receptors: Vascular and Cardiac Effects in Hypertension Hypertension, October 1, 2003; 42(4): 664 - 668. [Abstract] [Full Text] [PDF]
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N. Satoh, Y. Ogawa, T. Usui, T. Tagami, S. Kono, H. Uesugi, H. Sugiyama, A. Sugawara, K. Yamada, A. Shimatsu, et al. Antiatherogenic Effect of Pioglitazone in Type 2 Diabetic Patients Irrespective of the Responsiveness to Its Antidiabetic Effect Diabetes Care, September 1, 2003; 26(9): 2493 - 2499. [Abstract] [Full Text] [PDF]
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N. Varo, D. Vicent, P. Libby, R. Nuzzo, A. L. Calle-Pascual, M. R. Bernal, A. Fernandez-Cruz, A. Veves, P. Jarolim, J. J. Varo, et al. Elevated Plasma Levels of the Atherogenic Mediator Soluble CD40 Ligand in Diabetic Patients: A Novel Target of Thiazolidinediones Circulation, June 3, 2003; 107(21): 2664 - 2669. [Abstract] [Full Text] [PDF]
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P. M. Ridker, N. R. Cook, S. Cheng, H. A. Erlich, K. Lindpaintner, J. Plutzky, and R. Y.L. Zee Alanine for Proline Substitution in the Peroxisome Proliferator-Activated Receptor Gamma-2 (PPARG2) Gene and the Risk of Incident Myocardial Infarction Arterioscler Thromb Vasc Biol, May 1, 2003; 23(5): 859 - 863. [Abstract] [Full Text] [PDF]
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G. G. L. Biondi-Zoccai, A. Abbate, G. Liuzzo, and L. M. Biasucci Atherothrombosis, inflammation, and diabetes J. Am. Coll. Cardiol., April 2, 2003; 41(7): 1071 - 1077. [Abstract] [Full Text] [PDF]
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Y. Hattori, M. Matsumura, and K. Kasai Vascular smooth muscle cell activation by C-reactive protein Cardiovasc Res, April 1, 2003; 58(1): 186 - 195. [Abstract] [Full Text] [PDF]
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C.-H. Wang, R. D. Weisel, P. P. Liu, P. W.M. Fedak, and S. Verma Glitazones and Heart Failure: Critical Appraisal for the Clinician Circulation, March 18, 2003; 107(10): 1350 - 1354. [Full Text] [PDF]
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O. Ziouzenkova, S. Perrey, L. Asatryan, J. Hwang, K. L. MacNaul, D. E. Moller, D. J. Rader, A. Sevanian, R. Zechner, G. Hoefler, et al. Lipolysis of triglyceride-rich lipoproteins generates PPAR ligands: Evidence for an antiinflammatory role for lipoprotein lipase PNAS, March 4, 2003; 100(5): 2730 - 2735. [Abstract] [Full Text] [PDF]
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N. Marx, J. Froehlich, L. Siam, J. Ittner, G. Wierse, A. Schmidt, H. Scharnagl, V. Hombach, and W. Koenig Antidiabetic PPAR{gamma}-Activator Rosiglitazone Reduces MMP-9 Serum Levels in Type 2 Diabetic Patients With Coronary Artery Disease Arterioscler Thromb Vasc Biol, February 1, 2003; 23(2): 283 - 288. [Abstract] [Full Text] [PDF]
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D. S. Calnek, L. Mazzella, S. Roser, J. Roman, and C. M. Hart Peroxisome Proliferator-Activated Receptor {gamma} Ligands Increase Release of Nitric Oxide From Endothelial Cells Arterioscler Thromb Vasc Biol, January 1, 2003; 23(1): 52 - 57. [Abstract] [Full Text] [PDF]
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M. Ishibashi, K. Egashira, K.-i. Hiasa, S. Inoue, W. Ni, Q. Zhao, M. Usui, S. Kitamoto, T. Ichiki, and A. Takeshita Antiinflammatory and Antiarteriosclerotic Effects of Pioglitazone Hypertension, November 1, 2002; 40(5): 687 - 693. [Abstract] [Full Text] [PDF]
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N. Wang, L. Verna, N.-G. Chen, J. Chen, H. Li, B. M. Forman, and M. B. Stemerman Constitutive Activation of Peroxisome Proliferator-activated Receptor-gamma Suppresses Pro-inflammatory Adhesion Molecules in Human Vascular Endothelial Cells J. Biol. Chem., September 6, 2002; 277(37): 34176 - 34181. [Abstract] [Full Text] [PDF]
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D. L. Bhatt and E. J. Topol Need to Test the Arterial Inflammation Hypothesis Circulation, July 2, 2002; 106(1): 136 - 140. [Full Text] [PDF]
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O. Barbier, I. P. Torra, Y. Duguay, C. Blanquart, J.-C. Fruchart, C. Glineur, and B. Staels Pleiotropic Actions of Peroxisome Proliferator-Activated Receptors in Lipid Metabolism and Atherosclerosis Arterioscler Thromb Vasc Biol, May 1, 2002; 22(5): 717 - 726. [Abstract] [Full Text] [PDF]
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T. E. Akiyama, S. Sakai, G. Lambert, C. J. Nicol, K. Matsusue, S. Pimprale, Y.-H. Lee, M. Ricote, C. K. Glass, H. B. Brewer Jr., et al. Conditional Disruption of the Peroxisome Proliferator-Activated Receptor {gamma} Gene in Mice Results in Lowered Expression of ABCA1, ABCG1, and apoE in Macrophages and Reduced Cholesterol Efflux Mol. Cell. Biol., April 15, 2002; 22(8): 2607 - 2619. [Abstract] [Full Text] [PDF]
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B. Molavi, N. Rasouli, and J. L. Mehta Peroxisome Proliferator-Activated Receptor Ligands as Antiatherogenic Agents: Panacea or Another Pandora's Box? Journal of Cardiovascular Pharmacology and Therapeutics, March 1, 2002; 7(1): 1 - 8. [Abstract] [PDF]
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B. R. Kwak, S. Myit, F. Mulhaupt, N. Veillard, N. Rufer, E. Roosnek, and F. Mach PPAR{gamma} but not PPAR{alpha} Ligands Are Potent Repressors of Major Histocompatibility Complex Class II Induction in Atheroma-Associated Cells Circ. Res., February 22, 2002; 90(3): 356 - 362. [Abstract] [Full Text] [PDF]
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D. P. Kelly The Pleiotropic Nature of the Vascular PPAR Gene Regulatory Pathway Circ. Res., November 23, 2001; 89(11): 935 - 937. [Full Text] [PDF]
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A.-L. Levonen, D. A. Dickinson, D. R. Moellering, R. T. Mulcahy, H. J. Forman, and V. M. Darley-Usmar Biphasic Effects of 15-Deoxy-{Delta}12,14-Prostaglandin J2 on Glutathione Induction and Apoptosis in Human Endothelial Cells Arterioscler Thromb Vasc Biol, November 1, 2001; 21(11): 1846 - 1851. [Abstract] [Full Text] [PDF]
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L. Serghides and K. C. Kain Peroxisome Proliferator-Activated Receptor {{gamma}}-Retinoid X Receptor Agonists Increase CD36-Dependent Phagocytosis of Plasmodium falciparum-Parasitized Erythrocytes and Decrease Malaria-Induced TNF-{{alpha}} Secretion by Monocytes/Macrophages J. Immunol., June 1, 2001; 166(11): 6742 - 6748. [Abstract] [Full Text] [PDF]
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V. Pasceri, J. Chang, J. T. Willerson, and E. T. H. Yeh Modulation of C-Reactive Protein-Mediated Monocyte Chemoattractant Protein-1 Induction in Human Endothelial Cells by Anti-Atherosclerosis Drugs Circulation, May 29, 2001; 103(21): 2531 - 2534. [Abstract] [Full Text] [PDF]
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A. R. Collins, W. P. Meehan, U. Kintscher, S. Jackson, S. Wakino, G. Noh, W. Palinski, W. A. Hsueh, and R. E. Law Troglitazone Inhibits Formation of Early Atherosclerotic Lesions in Diabetic and Nondiabetic Low Density Lipoprotein Receptor-Deficient Mice Arterioscler Thromb Vasc Biol, March 1, 2001; 21(3): 365 - 371. [Abstract] [Full Text] [PDF]
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Z. Chen, S. Ishibashi, S. Perrey, J.-i. Osuga, T. Gotoda, T. Kitamine, Y. Tamura, H. Okazaki, N. Yahagi, Y. Iizuka, et al. Troglitazone Inhibits Atherosclerosis in Apolipoprotein E-Knockout Mice : Pleiotropic Effects on CD36 Expression and HDL Arterioscler Thromb Vasc Biol, March 1, 2001; 21(3): 372 - 377. [Abstract] [Full Text] [PDF]
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T. Claudel, M. D. Leibowitz, C. Fiévet, A. Tailleux, B. Wagner, J. J. Repa, G. Torpier, J.-M. Lobaccaro, J. R. Paterniti, D. J. Mangelsdorf, et al. Reduction of atherosclerosis in apolipoprotein E knockout mice by activation of the retinoid X receptor PNAS, February 15, 2001; (2001) 41609298. [Abstract] [Full Text]
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C. S. Elangbam, R. D. Tyler, and R. M. Lightfoot Peroxisome Proliferator-activated Receptors in Atherosclerosis and Inflammation--An Update Toxicol Pathol, February 1, 2001; 29(2): 224 - 231. [Abstract] [PDF]
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W. A. Hsueh, S. Jackson, and R. E. Law Control of Vascular Cell Proliferation and Migration by PPAR-{gamma}: A new approach to the macrovascular complications of diabetes Diabetes Care, February 1, 2001; 24(2): 392 - 397. [Abstract] [Full Text]
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V. Pasceri, J. T. Willerson, and E. T. H. Yeh Direct Proinflammatory Effect of C-Reactive Protein on Human Endothelial Cells Circulation, October 31, 2000; 102(18): 2165 - 2168. [Abstract] [Full Text] [PDF]
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T. Claudel, M. D. Leibowitz, C. Fievet, A. Tailleux, B. Wagner, J. J. Repa, G. Torpier, J.-M. Lobaccaro, J. R. Paterniti, D. J. Mangelsdorf, et al. Reduction of atherosclerosis in apolipoprotein E knockout mice by activation of the retinoid X receptor PNAS, February 27, 2001; 98(5): 2610 - 2615. [Abstract] [Full Text] [PDF]
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B. R. Kwak, S. Myit, F. Mulhaupt, N. Veillard, N. Rufer, E. Roosnek, and F. Mach PPAR{gamma} but not PPAR{alpha} Ligands Are Potent Repressors of Major Histocompatibility Complex Class II Induction in Atheroma-Associated Cells Circ. Res., February 22, 2002; 90(3): 356 - 362. [Abstract] [Full Text] [PDF]
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