(Circulation. 2001;103:1772.)
© 2001 American Heart Association, Inc.
Basic Science Reports |
RANTES Deposition by Platelets Triggers Monocyte Arrest on Inflamed and Atherosclerotic Endothelium
From the Institut für Prophylaxe der Kreislaufkrankheiten (P.v.H., K.S.C.W., C.W.) and Medizinische Poliklinik (P.J.N., C.W.), Ludwig-Maximilians-Universität, Munich, Germany; the Department of Biomedical Engineering (Y.H., K.L.), University of Virginia, Charlottesville; and the Serono Pharmaceutical Research Institute (A.E.I.P.), Geneva, Switzerland.
Correspondence to C. Weber, Institut für Prophylaxe der Kreislaufkrankheiten, Pettenkoferstrasse 9, 80336 München, Germany. E-mail christian.weber{at}klp.med.uni-muenchen.de
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Abstract |
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 Top Abstract IntroductionMethodsResults and DiscussionReferences |
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Background—Circulating platelets and chemoattractant proteins, such as the CC chemokine RANTES, contribute to the activation and interaction of monocytes and endothelium and may thereby play a pivotal role in the pathogenesis of inflammatory and atherosclerotic disease.
Methods and Results—The binding of RANTES to human endothelial cells was detected by ELISA or immunofluorescence after perfusion with platelets or exposure to their supernatants. Monocyte arrest on endothelial monolayers or surface-adherent platelets was studied with a parallel-wall flow chamber and video microscopy. We show that RANTES secreted by thrombin-stimulated platelets is immobilized on the surface of inflamed microvascular or aortic endothelium and triggers shear-resistant monocyte arrest under flow conditions, as shown by inhibition with the RANTES receptor antagonist Met-RANTES or a blocking RANTES antibody. Deposition of RANTES and its effects requires endothelial activation, eg, by interleukin-1ß, and is not supported by venous endothelium or adherent platelets. Immunohistochemistry revealed that RANTES is present on the luminal surface of carotid arteries of apolipoprotein E–deficient mice with early atherosclerotic lesions after wire-induced injury or cytokine exposure. In a mechanistic model of atherogenesis, monocyte adherence on endothelium covering such lesions was studied in murine carotid arteries perfused ex vivo, showing that the accumulation of monocytic cells in these carotid arteries involved RANTES receptors.
Conclusions—The deposition of RANTES by platelets triggers shear-resistant monocyte arrest on inflamed or atherosclerotic endothelium. Delivery of RANTES by platelets may epitomize a novel principle relevant to inflammatory or atherogenic monocyte recruitment from the circulation.
Key Words: inflammation • atherosclerosis • platelets • peptides • monocytes • blood flow
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Introduction |
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TopAbstractIntroductionMethodsResults and DiscussionReferences |
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Activation of vascular endothelium during the pathogenesis of inflammatory conditions, such as atherosclerosis or transplant rejection, leads to a subintimal infiltration with monocytes that is thought to be orchestrated by the sequential involvement of multiple signal molecules, eg, chemokines and their monocyte receptors.1 2 Induction of the chemokine monocyte chemotactic protein-1 (MCP-1) is evident in macrophage-rich atherosclerotic lesions.3 4 MCP-1, its receptor CCR2, and the growth-related activity (GRO)-
receptor
CXCR2 contribute to macrophage infiltration and lesion formation in
atherosclerosis-prone mouse
models.5 6 7
CXC chemokines, such as interleukin (IL)-8 or GRO-
immobilized to heparan proteoglycans on inflamed endothelium, and MCP-1
can mediate the shear-resistant arrest of monocytes via their receptors
and may also be involved in subsequent spreading and
emigration.8 9 10
The CC chemokine RANTES, which has been found in arteries with
transplant atherosclerosis and has been implicated in allograft
rejection,11 12
can bind to microvascular endothelium and trigger monocyte arrest under
flow
conditions. Circulating platelets may affect vascular and inflammatory syndromes by bridging between endothelium and monocytes or via their secretory products.1 Their cooperative cellular interactions are mediated by adhesion molecules, ie, P-selectin or ß2- and ß3-integrins binding to fibrinogen, and contribute to thrombus formation and fibrin deposition.13 14 15 16 On activation, platelets express surface-bound molecules and release of proinflammatory cytokines, eg, IL-1ß, resulting in endothelial activation, and secrete chemoattractants, eg, platelet-activating factor (PAF) and RANTES.17 18 19 20 Given the crucial role of chemokines in coordinating leukocyte traffic, we tested whether platelets may be involved in monocyte recruitment due to delivery and deposition of chemokines to inflamed endothelium.
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Methods |
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TopAbstractIntroductionMethodsResults and DiscussionReferences |
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Cell Culture, Cell Isolation, and Reagents
Human microvascular endothelial cells (HMVECs), human aortic endothelial cells (HAECs) (both Clonetics), human umbilical vein endothelial cells (HUVECs), or Mono Mac 6 cells were cultured as described.8 12 Monocytes were isolated from leukocyte-rich plasma by hyperosmotic NycoPrep 1.068 density gradient centrifugation (Nycomed), yielding a purity of 80% to 85% unactivated cells.21 Platelets were isolated by centrifugation of platelet-rich plasma13 on a 40% human serum albumin (HSA) cushion at 1200g and Sepharose-2B (Pharmacia) gel filtration of the interface and kept in HHMC (HBSS, 10 mmol/L HEPES, 1 mmol/L Ca2+ and Mg2+, 0.5% HSA) at 37°C. Flow cytometry of surface P-selectin revealed that platelets were not activated (not shown). The RANTES receptor antagonist Met-RANTES generated by retention of the initiation methionine,22 PAF antagonist L-659,989 (MS&D),23 and monoclonal antibody (mAb) VL-1 to RANTES24 have been described. P-selectin mAb AK-4 was from Pharmingen, and goat polyclonal Abs to murine RANTES (C-19) or MCP-1 (R-17) were from Santa Cruz. Recombinant RANTES, IL-1ß, and murine tumor necrosis factor (TNF)-
were from PeproTech. Other reagents were from Sigma Chemical
Co.
Monocyte Recruitment on Endothelium or Adherent
Platelets in Shear Flow
Laminar flow assays were performed as
described.8 13 25
Confluent ECs activated with IL-1ß (10 ng/mL) for 12 hours or
surface-adherent platelet layers formed by binding to silane-treated
glass slides13 and activated
with thrombin were assembled as the lower wall of a flow chamber on the
stage of an Olympus IMT-2 microscope. Endothelium was preperfused at a
shear rate of 1.5 dyne/cm2 or preincubated
in stasis with platelets (108 cells/mL) or
supernatants for 20 minutes at 37°C after platelet stimulation with
thrombin (0.5 U/mL) for 5 minutes. Preexposure to platelets or
supernatants was also performed in the presence of the blocking RANTES
mAb VL-1 (10 µg/mL). An isotype control mAb had no effect (not
shown). Mono Mac 6 cells or monocytes (106
cells/mL) were resuspended and pretreated with Met-RANTES (1 µg/mL)
for 15 minutes in HHMC
(Mg2+/Ca2+ added
shortly before assays), kept at 37°C during assays, and perfused at
1.5 dyne/cm2. The number of monocytes firmly
adherent by primary interaction with endothelium after 5 minutes of
accumulation was quantified in multiple fields by analysis of
images recorded with a JVC 3CCD video camera and recorder. Data were
analyzed by ANOVA.
ELISA, Flow Cytometry, and
Immunofluorescence
Detection of soluble or surface-adherent RANTES was
performed by a modified ELISA as
described.12 For flow
cytometry,12 platelets were
reacted with P-selectin mAb AK-4, RANTES mAb VL-1, or isotype controls
(10 µg/mL) in HHMC with 0.5% BSA for 30 minutes, stained with
FITC-conjugated goat anti-mouse IgG mAb for 30 minutes on ice, and
analyzed in a FACScan (Becton Dickinson). Immunofluorescence was
performed as described.8
Briefly, HMVECs grown on glass coverslips were activated with IL-1ß
and treated as above, fixed in 3.7% formaldehyde, and incubated for 2
hours at room temperature with 10% heat-inactivated HSA in PBS to
block nonspecific binding. Cells were reacted with VL-1 mAb overnight
at 4°C and incubated with FITC-conjugated IgG for 30 minutes at
25°C. Images were recorded with a Leica DMRBE fluorescence microscope
with an x100 oil immersion objective.
Immunohistochemistry and Ex Vivo Perfusion of
Murine Carotid Arteries
Carotid arteries from
apoE-/- mice (Jackson Laboratories, Bar
Harbor, Me) fed a Western-type diet (21% fat) for 5 weeks or
from C57BL/6 mice (Hilltop, Scottdale, Pa) were paraffin-embedded and
cut into 5-µm sections (3 to 4 mice per treatment). Some
apoE-/- mice were wire-injured as
reported,26 and some mice
were treated with TNF- (1 µg IP) 4 hours before the artery was
harvested. Endogenous peroxidase was blocked with 0.45%
H2O2 in methanol.
Antigens were retrieved by boiling slides in unmasking solution. Slides
were allowed to cool and were blocked in buffer containing fish skin
oil gelatin, normal horse serum (5%), and an avidin-blocking agent
(all Vector Laboratories) to reduce unspecific background staining. For
staining, slides were incubated with goat polyclonal Ab C-19 (1.5
µg/mL) or R-17 (1 µg/mL), 5% normal horse serum, and biotin at
4°C overnight, reacted with biotinylated secondary horse anti-goat
Ab, avidin-biotin peroxidase complex, and 3,3'-diaminobenzidine
substrate. Slides were counterstained with hematoxylin, dehydrated with
xylene, and mounted, and images were recorded. Perfusion of carotid
arteries from apoE-/- mice ex vivo was
performed as described.27
Arteries were infused with or without RANTES (150 ng/mL) for 30 minutes
and washed. Mono Mac 6 cells treated with or without pertussis toxin
(PTX) (200 ng/mL) were labeled with calcein (0.5 µg/mL, Molecular
Probes), resuspended at 3x106 cells/mL, and
pretreated with Met-RANTES (1 µg/mL) for 15 minutes. Suspensions were
perfused in isolated carotid arteries at 10 µL/min. Perfusion and
accumulation of labeled monocytic cells were observed by stroboscopic
epifluorescence illumination (Strobex; Chadwick-Helmuth) by intravital
microscopy (Axioskop FS; Carl Zeiss) with an SW20 immersion
objective.
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Results and Discussion |
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TopAbstractIntroductionMethodsResults and DiscussionReferences |
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RANTES Triggers Monocyte Arrest on Endothelium Preconditioned by Platelets
To investigate whether platelets or their secretory products "prime" endothelium to support initial monocyte arrest, endothelial monolayers activated with IL-1ß were exposed to resting or thrombin-stimulated platelets in stasis or at low shear or were preincubated with their supernatants. Subsequently, human monocytic Mono Mac 6 cells were perfused at a shear rate of 1.5 dyne/cm2, and cells adherent primarily to endothelium were counted after 5 minutes of accumulation. Exposure of activated HMVECs to thrombin-stimulated platelets by preperfusion or in stasis triggered a 2-fold increase in shear-resistant monocytic cell arrest (Figure 1A
). Preincubation of activated HMVECs with
supernatants from thrombin-stimulated platelets, but not thrombin alone
or resting platelets, was sufficient to increase arrest
(Figure 1A). This implicates soluble platelet products and
excludes direct effects of thrombin.
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Because platelets release RANTES on stimulation and
degranulation,20 we studied
its role in monocyte arrest on HMVECs primed by platelets. Pretreatment
of monocytic cells with a peptide RANTES receptor antagonist,
Met-RANTES,22 abolished firm
arrest induced by exposure to stimulated platelets or supernatants
(Figure 1A
). Similar inhibition was achieved by preincubation
of HMVECs in the presence of a blocking RANTES mAb
(Figure 1A) but not with an MCP-1 peptide antagonist. This
reveals the involvement of monocytic RANTES receptors and indicates
that the secreted platelet product mediating arrest is RANTES. The
increase in monocyte adhesion after pretreatment with stimulated
platelets was observed only on IL-1ß–activated HMVECs but not on
resting HMVECs, which support only minimal adhesion (data not shown).
In contrast, exposure of IL-1ß–activated HUVECs to platelets or
their supernatants did not affect monocytic cell arrest
(Figure 1B). The fact that binding of RANTES is clearly
detectable on activated HMVECs but not on resting HMVECs or
activated HUVECs (Reference 1212 ; P.J.N., unpublished data) suggests that
cytokine activation is necessary for binding of RANTES to HMVECs and
that cell type–specific immobilization of RANTES is required for its
function. Experiments performed with isolated human blood monocytes
confirmed that Met-RANTES inhibited arrest on HMVECs when primed by
exposure to stimulated platelets or supernatants
(Figure 1C). Moreover, preperfusion of IL-1ß–activated
HAECs with stimulated platelets or exposure to their supernatants
triggered monocyte arrest that was blocked by Met-RANTES
(Figure 1D), extending the relevance of our results to the
arterial macrovasculature. Thus, RANTES released by platelets and bound
to the surface of inflamed endothelium supports monocyte arrest in
flow.
Surface Binding of Platelet-Derived
RANTES to Activated Endothelium
We next studied whether RANTES secreted by
stimulated platelets is deposited on HMVECs. ELISA confirmed that after
stimulation, platelets released substantial amounts of RANTES into
supernatants
(Figure 2A). Flow cytometry detected a marked
expression of P-selectin but not RANTES on the surface of
thrombin-stimulated platelets
(Figure 2B). Cell surface ELISA, however, demonstrated that
incubation of IL-1ß–activated HMVECs or HAECs with
thrombin-stimulated but not resting platelets or supernatants under
rotation resulted in a solid immobilization of RANTES but not MCP-1 to
the surface of HMVECs or HAECs but not of resting HMVECs or resting or
activated HUVECs
(Figure 2C). These observations support the conclusion that
cytokine activation is necessary to induce specific endothelial binding
sites for RANTES. Immunofluorescence analysis of IL-1ß–activated
HMVECs confirmed that preperfusion with resting platelets did not
result in specific staining for RANTES
(Figure 2D). After exposure of HMVECs to thrombin-stimulated
platelets in shear flow, an intense staining was observed
(Figure 2D), indicating substantial immobilization of RANTES
on the endothelial surface. Deposition after platelet preperfusion
appeared to be more pronounced than after incubation with platelets or
supernatants in stasis
(Figure 2D). This may imply a potential role for signals
promoting degranulation of platelets in flow.
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RANTES Is Not Involved in Monocyte
Arrest on Adherent Platelets
Platelets may also be important for leukocyte
recruitment when adherent to surfaces exposed by endothelial injury or
denudation. Accumulation of neutrophils on stimulated platelets in
shear flow involved activation of the
ß2-integrin Mac-1 by the lipid mediator PAF
but not chemokines acting via
CXCR2.13 Similarly, the PAF
antagonist L-659,98923 but
not Met-RANTES inhibited monocyte arrest on thrombin-stimulated
platelet layers in shear flow
(Figure 2E). This is most likely due to an inability of
platelets to bind RANTES, whereas PAF is retained in lipid
membranes.13 Thus,
monocyte-platelet interactions in shear flow are triggered by PAF,
whereas RANTES secreted by platelets is insufficient to support arrest
unless immobilized by activated endothelium.
Luminal Deposition of RANTES in
Atherosclerotic and Injured Arteries
RANTES expression has been detected on endothelium of
coronary arteries undergoing transplant-associated accelerated
atherosclerosis.11 To assess
the relevance of RANTES deposition in the context of atherogenesis in
vivo, immunohistochemistry was performed after wire-induced injury on
carotid arteries from lesion-prone
apoE-/- mice fed a western diet and from
wild-type mice treated with TNF-. RANTES was detectable in the
intima and media (eg, in mononuclear cell infiltrates) of early
atherosclerotic lesions in apoE-/- mice;
most accentuated staining, however, was seen on the luminal surface of
the arterial wall, within thrombotic material juxtaposed to the lesions
and possibly in association with the endothelium
(Figure 3A). A similar pattern of staining for RANTES was
found in human carotid atherectomy specimens with advanced lesions (not
shown). The finding that in situ hybridization did not reveal RANTES
mRNA in inflamed
endothelium28 suggests
paracrine delivery of RANTES to such sites. By contrast, no staining
for RANTES was observed in carotid arteries of
apoE+/+ mice
(Figure 3B) or with isotype control
(Figure 3C). Four weeks after a wire-induced injury to the
carotid artery of apoE-/-
mice,29 selective RANTES
staining was found on the surface lining of the neointimal lesions
(Figure 3D). Stimulation with TNF- resulted in marked
RANTES staining throughout the intima and media of wild-type carotid
arteries
(Figure 3E). MCP-1 was also found in monocyte/macrophage-rich
areas of lesions in apoE-/- mice
(Figure 3F). All observations were obtained consistently in
3 animals.
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Monocyte Arrest in Carotid Arteries of
ApoE-/- Mice Involves RANTES
Receptors
In a mechanistic investigation of macrophage
recruitment in atherogenesis, monocytic cells perfused ex vivo have
been shown to accumulate on endothelium covering early atherosclerotic
lesions in carotid arteries from apoE-/-
mice.27 In this model,
attachment of Mono Mac 6 cells was reduced by Met-RANTES (data not
shown) but increased by preinfusion of arteries with RANTES
(Figure 4). Pretreatment with PTX resulted in a 50%
inhibition of monocyte arrest, confirming that it was mediated by
Gi protein–dependent and –independent
mechanisms
(Figure 4). An equivalent inhibition with Met-RANTES
indicated that PTX-sensitive arrest was mediated largely by RANTES
receptors
(Figure 4). The PTX-insensitive component was blocked by
4 mAb (data not shown), reflecting the
presence of preactivated 4
integrins.27 Because
efficient cross-species responses of human monocytes in murine vessels
are conceivable, given the structural and functional conservation of
RANTES,30 our data suggest
that RANTES receptors are involved in atherogenic monocyte
recruitment.
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Implications of Platelet-Derived RANTES for
Inflammation and Vascular Disease
Studies on the role of platelets in
monocyte recruitment have been based largely on their direct
interactions. Our data provide the first evidence that the conveyance
of RANTES by platelets and its deposition on the endothelial surface
can trigger monocyte arrest to inflamed endothelium of microvascular or
arterial origin. Although potential effects of less abundant platelet
chemokines or precursors cannot be excluded, our results clearly
implicate RANTES and its receptors. This mechanism thus defines a novel
principle by which platelets support inflammatory recruitment of
monocytes from the circulation in distinct vascular beds, epitomizing a
proximal step in an emerging
hierarchy.8 The presence of
RANTES on the luminal surface of diseased or injured carotid arteries
further implies that this concept is relevant for the direct
recruitment of monocytes to atherosclerotic or restenotic lesions. In
light of the crucial and complex involvement of monocytes in
atherogenesis,1 blocking
platelet-derived RANTES as a culprit for monocyte arrest with peptide
analogues, such as Met-RANTES, or selective nonpeptide receptor
antagonists may thus serve as a future approach to the prevention and
therapy of atherosclerosis and
restenosis.
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Acknowledgments |
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This work was supported by Deutsche Forschungsgemeinschaft grants We-1913/2-1 and 2-2 (Dr C. Weber), GrK-438 (Drs C. Weber, K. Weber, and Nelson), and SFB-464 and 469 (Dr Nelson) and NIH grant HL-58108 (Dr Ley). We thank P.C. Weber and D. Schlöndorff for continuous support, D.R. Manka for help with the animal experiments, C. Klier for endothelial cell culture, and J. Sanders for expert help with immunohistochemistry. This work in part fulfills requirements for the doctoral dissertation of P. von Hundelshausen.
Received July 5, 2000; revision received October 16, 2000; accepted October 27, 2000.
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S. Terao, G. Yilmaz, K. Y. Stokes, J. Russell, M. Ishikawa, T. Kawase, and D. N. Granger Blood Cell-Derived RANTES Mediates Cerebral Microvascular Dysfunction, Inflammation, and Tissue Injury After Focal Ischemia-Reperfusion Stroke, September 1, 2008; 39(9): 2560 - 2570. [Abstract] [Full Text] [PDF]
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 D. D. Wagner and P. S. Frenette The vessel wall and its interactions Blood, June 1, 2008; 111(11): 5271 - 5281. [Abstract] [Full Text] [PDF]
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N. Li Platelet-lymphocyte cross-talk J. Leukoc. Biol., May 1, 2008; 83(5): 1069 - 1078. [Abstract] [Full Text] [PDF]
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 C. N. Morrell, K. Murata, A. M. Swaim, E. Mason, T. V. Martin, L. E. Thompson, M. Ballard, K. Fox-Talbot, B. Wasowska, and W. M. Baldwin III In Vivo Platelet-Endothelial Cell Interactions in Response to Major Histocompatibility Complex Alloantibody Circ. Res., April 11, 2008; 102(7): 777 - 785. [Abstract] [Full Text] [PDF]
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A. Mueller, A. Meiser, E. M. McDonagh, J. M. Fox, S. J. Petit, G. Xanthou, T. J. Williams, and J. E. Pease CXCL4-induced migration of activated T lymphocytes is mediated by the chemokine receptor CXCR3 J. Leukoc. Biol., April 1, 2008; 83(4): 875 - 882. [Abstract] [Full Text] [PDF]
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R. Pasvolsky, V. Grabovsky, C. Giagulli, Z. Shulman, R. Shamri, S. W. Feigelson, C. Laudanna, and R. Alon RhoA Is Involved in LFA-1 Extension Triggered by CXCL12 but Not in a Novel Outside-In LFA-1 Activation Facilitated by CXCL9 J. Immunol., March 1, 2008; 180(5): 2815 - 2823. [Abstract] [Full Text] [PDF]
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 G. Davi and C. Patrono Platelet Activation and Atherothrombosis N. Engl. J. Med., December 13, 2007; 357(24): 2482 - 2494. [Full Text] [PDF]
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Y. N. A. Nabah, M. Losada, R. Estelles, T. Mateo, C. Company, L. Piqueras, C. Lopez-Gines, H. Sarau, J. Cortijo, E. J. Morcillo, et al. CXCR2 Blockade Impairs Angiotensin II Induced CC Chemokine Synthesis and Mononuclear Leukocyte Infiltration Arterioscler Thromb Vasc Biol, November 1, 2007; 27(11): 2370 - 2376. [Abstract] [Full Text] [PDF]
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E. Galkina, B. L. Harry, A. Ludwig, E. A. Liehn, J. M. Sanders, A. Bruce, C. Weber, and K. Ley CXCR6 Promotes Atherosclerosis by Supporting T-Cell Homing, Interferon-{gamma} Production, and Macrophage Accumulation in the Aortic Wall Circulation, October 16, 2007; 116(16): 1801 - 1811. [Abstract] [Full Text] [PDF]
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 M. B. Rookmaaker, M. C. Verhaar, H. C. de Boer, R. Goldschmeding, J. A. Joles, H. A. Koomans, H.-J. Grone, and T. J. Rabelink Met-RANTES reduces endothelial progenitor cell homing to activated (glomerular) endothelium in vitro and in vivo Am J Physiol Renal Physiol, August 1, 2007; 293(2): F624 - F630. [Abstract] [Full Text] [PDF]
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 C. A. Gleissner, N. Leitinger, and K. Ley Effects of Native and Modified Low-Density Lipoproteins on Monocyte Recruitment in Atherosclerosis Hypertension, August 1, 2007; 50(2): 276 - 283. [Full Text] [PDF]
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S. Danese, E. Dejana, and C. Fiocchi Immune Regulation by Microvascular Endothelial Cells: Directing Innate and Adaptive Immunity, Coagulation, and Inflammation J. Immunol., May 15, 2007; 178(10): 6017 - 6022. [Abstract] [Full Text] [PDF]
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R. R. Koenen, P. von Hundelshausen, and C. Weber Inflammatory Blues Turns Velvet Skin Into Rawhide: Monocyte Rolling on Modified Endothelial PSGL-1 Arterioscler Thromb Vasc Biol, May 1, 2007; 27(5): 990 - 992. [Full Text] [PDF]
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L. Zhang, K. Peppel, P. Sivashanmugam, E. S. Orman, L. Brian, S. T. Exum, and N. J. Freedman Expression of Tumor Necrosis Factor Receptor-1 in Arterial Wall Cells Promotes Atherosclerosis Arterioscler Thromb Vasc Biol, May 1, 2007; 27(5): 1087 - 1094. [Abstract] [Full Text] [PDF]
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R. N. Mitchell and P. Libby Vascular Remodeling in Transplant Vasculopathy Circ. Res., April 13, 2007; 100(7): 967 - 978. [Abstract] [Full Text] [PDF]
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E. Cavusoglu, C. Eng, V. Chopra, L. T. Clark, D. J. Pinsky, and J. D. Marmur Low Plasma RANTES Levels Are an Independent Predictor of Cardiac Mortality in Patients Referred for Coronary Angiography Arterioscler Thromb Vasc Biol, April 1, 2007; 27(4): 929 - 935. [Abstract] [Full Text] [PDF]
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P. von Hundelshausen and C. Weber Platelets as Immune Cells: Bridging Inflammation and Cardiovascular Disease Circ. Res., January 5, 2007; 100(1): 27 - 40. [Abstract] [Full Text] [PDF]
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O. Morel, F. Toti, B. Hugel, B. Bakouboula, L. Camoin-Jau, F. Dignat-George, and J.-M. Freyssinet Procoagulant Microparticles: Disrupting the Vascular Homeostasis Equation? Arterioscler Thromb Vasc Biol, December 1, 2006; 26(12): 2594 - 2604. [Abstract] [Full Text] [PDF]
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T. Heitzer, V. Rudolph, E. Schwedhelm, M. Karstens, K. Sydow, M. Ortak, P. Tschentscher, T. Meinertz, R. Boger, and S. Baldus Clopidogrel Improves Systemic Endothelial Nitric Oxide Bioavailability in Patients With Coronary Artery Disease: Evidence for Antioxidant and Antiinflammatory Effects Arterioscler Thromb Vasc Biol, July 1, 2006; 26(7): 1648 - 1652. [Abstract] [Full Text] [PDF]
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S. Fujimi, M. P. MacConmara, A. A. Maung, Y. Zang, J. A. Mannick, J. A. Lederer, and P. H. Lapchak Platelet depletion in mice increases mortality after thermal injury Blood, June 1, 2006; 107(11): 4399 - 4406. [Abstract] [Full Text] [PDF]
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 J. P. Mathew, H. M. Rinder, B. R. Smith, M. F. Newman, and C. S. Rinder Transcerebral Platelet Activation After Aortic Cross-Clamp Release is Linked to Neurocognitive Decline. Ann. Thorac. Surg., May 1, 2006; 81(5): 1644 - 1649. [Abstract] [Full Text] [PDF]
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T. Mateo, Y. Naim Abu Nabah, M. Abu Taha, M. Mata, M. Cerda-Nicolas, A. E. I. Proudfoot, R. A. K. Stahl, A. C. Issekutz, J. Cortijo, E. J. Morcillo, et al. Angiotensin II-Induced Mononuclear Leukocyte Interactions with Arteriolar and Venular Endothelium Are Mediated by the Release of Different CC Chemokines J. Immunol., May 1, 2006; 176(9): 5577 - 5586. [Abstract] [Full Text] [PDF]
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 A. Tedgui and Z. Mallat Cytokines in Atherosclerosis: Pathogenic and Regulatory Pathways Physiol Rev, April 1, 2006; 86(2): 515 - 581. [Abstract] [Full Text] [PDF]
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 B. P. O'Sullivan and A. D. Michelson The Inflammatory Role of Platelets in Cystic Fibrosis Am. J. Respir. Crit. Care Med., March 1, 2006; 173(5): 483 - 490. [Abstract] [Full Text] [PDF]
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A. Zernecke, E. A. Liehn, L. Fraemohs, P. von Hundelshausen, R. R. Koenen, M. Corada, E. Dejana, and C. Weber Importance of Junctional Adhesion Molecule-A for Neointimal Lesion Formation and Infiltration in Atherosclerosis-Prone Mice Arterioscler Thromb Vasc Biol, February 1, 2006; 26(2): e10 - e13. [Abstract] [Full Text] [PDF]
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 E. Galkina and K. Ley Leukocyte Recruitment and Vascular Injury in Diabetic Nephropathy J. Am. Soc. Nephrol., February 1, 2006; 17(2): 368 - 377. [Abstract] [Full Text] [PDF]
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S. P. Tull, S. I. Anderson, S. C. Hughan, S. P. Watson, G. B. Nash, and G. E. Rainger Cellular Pathology of Atherosclerosis: Smooth Muscle Cells Promote Adhesion of Platelets to Cocultured Endothelial Cells Circ. Res., January 6, 2006; 98(1): 98 - 104. [Abstract] [Full Text] [PDF]
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 M. Notohamiprodjo, R. Djafarzadeh, A. Mojaat, I. von Luttichau, H.-J. Grone, and P. J. Nelson Generation of GPI-linked CCL5 based chemokine receptor antagonists for the suppression of acute vascular damage during allograft transplantation Protein Eng. Des. Sel., January 1, 2006; 19(1): 27 - 35. [Abstract] [Full Text] [PDF]
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D. Rothenbacher, S. Muller-Scholze, C. Herder, W. Koenig, and H. Kolb Differential Expression of Chemokines, Risk of Stable Coronary Heart Disease, and Correlation with Established Cardiovascular Risk Markers Arterioscler Thromb Vasc Biol, January 1, 2006; 26(1): 194 - 199. [Abstract] [Full Text] [PDF]
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K. B. Holven, J. K. Damas, A. Yndestad, T. Waehre, T. Ueland, B. Halvorsen, L. Heggelund, W. J. Sandberg, A. G. Semb, S. S. Froland, et al. Chemokines in Children With Heterozygous Familiar Hypercholesterolemia: Selective Upregulation of RANTES Arterioscler Thromb Vasc Biol, January 1, 2006; 26(1): 200 - 205. [Abstract] [Full Text] [PDF]
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 D. A. Vorchheimer and R. Becker Platelets in Atherothrombosis Mayo Clin. Proc., January 1, 2006; 81(1): 59 - 68. [Abstract] [Full Text] [PDF]
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E. J.A. van Wanrooij, H. Happe, A. D. Hauer, P. de Vos, T. Imanishi, H. Fujiwara, T. J.C. van Berkel, and J. Kuiper HIV Entry Inhibitor TAK-779 Attenuates Atherogenesis in Low-Density Lipoprotein Receptor-Deficient Mice Arterioscler Thromb Vasc Biol, December 1, 2005; 25(12): 2642 - 2647. [Abstract] [Full Text] [PDF]
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 M. Ellis, B. al-Ramadi, U. Hedstrom, H. Alizadeh, V. Shammas, and J. Kristensen Invasive fungal infections are associated with severe depletion of circulating RANTES J. Med. Microbiol., November 1, 2005; 54(11): 1017 - 1022. [Abstract] [Full Text] [PDF]
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V. S. Dole, W. Bergmeier, H. A. Mitchell, S. C. Eichenberger, and D. D. Wagner Activated platelets induce Weibel-Palade-body secretion and leukocyte rolling in vivo: role of P-selectin Blood, October 1, 2005; 106(7): 2334 - 2339. [Abstract] [Full Text] [PDF]
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S. Massberg, K. Schurzinger, M. Lorenz, I. Konrad, C. Schulz, N. Plesnila, E. Kennerknecht, M. Rudelius, S. Sauer, S. Braun, et al. Platelet Adhesion Via Glycoprotein IIb Integrin Is Critical for Atheroprogression and Focal Cerebral Ischemia: An In Vivo Study in Mice Lacking Glycoprotein IIb Circulation, August 23, 2005; 112(8): 1180 - 1188. [Abstract] [Full Text] [PDF]
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T. Baltus, P. von Hundelshausen, S. F. Mause, W. Buhre, R. Rossaint, and C. Weber Differential and additive effects of platelet-derived chemokines on monocyte arrest on inflamed endothelium under flow conditions J. Leukoc. Biol., August 1, 2005; 78(2): 435 - 441. [Abstract] [Full Text] [PDF]
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K. Wang, X. Zhou, Z. Zhou, N. Mal, L. Fan, M. Zhang, A. M. Lincoff, E. F. Plow, E. J. Topol, and M. S. Penn Platelet, Not Endothelial, P-Selectin Is Required for Neointimal Formation After Vascular Injury Arterioscler Thromb Vasc Biol, August 1, 2005; 25(8): 1584 - 1589. [Abstract] [Full Text] [PDF]
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S. F. Mause, P. von Hundelshausen, A. Zernecke, R. R. Koenen, and C. Weber Platelet Microparticles: A Transcellular Delivery System for RANTES Promoting Monocyte Recruitment on Endothelium Arterioscler Thromb Vasc Biol, July 1, 2005; 25(7): 1512 - 1518. [Abstract] [Full Text] [PDF]
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O. Soehnlein, X. Xie, H. Ulbrich, E. Kenne, P. Rotzius, H. Flodgaard, E. E. Eriksson, and L. Lindbom Neutrophil-Derived Heparin-Binding Protein (HBP/CAP37) Deposited on Endothelium Enhances Monocyte Arrest under Flow Conditions J. Immunol., May 15, 2005; 174(10): 6399 - 6405. [Abstract] [Full Text] [PDF]
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C. Weber Platelets and Chemokines in Atherosclerosis: Partners in Crime Circ. Res., April 1, 2005; 96(6): 612 - 616. [Abstract] [Full Text] [PDF]
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G. Ostermann, L. Fraemohs, T. Baltus, A. Schober, M. Lietz, A. Zernecke, E. A. Liehn, and C. Weber Involvement of JAM-A in Mononuclear Cell Recruitment on Inflamed or Atherosclerotic Endothelium: Inhibition by Soluble JAM-A Arterioscler Thromb Vasc Biol, April 1, 2005; 25(4): 729 - 735. [Abstract] [Full Text] [PDF]
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 S.-P. Gravel and M. J. Servant Roles of an I{kappa}B Kinase-related Pathway in Human Cytomegalovirus-infected Vascular Smooth Muscle Cells: A MOLECULAR LINK IN PATHOGEN-INDUCED PROATHEROSCLEROTIC CONDITIONS J. Biol. Chem., March 4, 2005; 280(9): 7477 - 7486. [Abstract] [Full Text] [PDF]
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P. von Hundelshausen, R. R. Koenen, M. Sack, S. F. Mause, W. Adriaens, A. E. I. Proudfoot, T. M. Hackeng, and C. Weber Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium Blood, February 1, 2005; 105(3): 924 - 930. [Abstract] [Full Text] [PDF]
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 M. J. Flick, X. Du, and J. L. Degen Fibrin(ogen)-{alpha}M{beta}2 Interactions Regulate Leukocyte Function and Innate Immunity In Vivo Experimental Biology and Medicine, December 1, 2004; 229(11): 1105 - 1110. [Abstract] [Full Text] [PDF]
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C. Weber, A. Schober, and A. Zernecke Chemokines: Key Regulators of Mononuclear Cell Recruitment in Atherosclerotic Vascular Disease Arterioscler Thromb Vasc Biol, November 1, 2004; 24(11): 1997 - 2008. [Abstract] [Full Text] [PDF]
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 E. Simeoni, B. R. Winkelmann, M. M. Hoffmann, S. Fleury, J. Ruiz, L. Kappenberger, W. Marz, and G. Vassalli Association of RANTES G-403A gene polymorphism with increased risk of coronary arteriosclerosis Eur. Heart J., August 2, 2004; 25(16): 1438 - 1446. [Abstract] [Full Text] [PDF]
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J. J. Yun, D. Whiting, M. P. Fischbein, A. Banerji, Y. Irie, D. Stein, M. C. Fishbein, A. E.I. Proudfoot, H. Laks, J. A. Berliner, et al. Combined Blockade of the Chemokine Receptors CCR1 and CCR5 Attenuates Chronic Rejection Circulation, February 24, 2004; 109(7): 932 - 937. [Abstract] [Full Text] [PDF]
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S. Danese, C. de la Motte, B. M. R. Reyes, M. Sans, A. D. Levine, and C. Fiocchi Cutting Edge: T Cells Trigger CD40-Dependent Platelet Activation and Granular RANTES Release: A Novel Pathway for Immune Response Amplification J. Immunol., February 15, 2004; 172(4): 2011 - 2015. [Abstract] [Full Text] [PDF]
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M. Gawaz Role of platelets in coronary thrombosis and reperfusion of ischemic myocardium Cardiovasc Res, February 15, 2004; 61(3): 498 - 511. [Abstract] [Full Text] [PDF]
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N. R. Veillard, B. Kwak, G. Pelli, F. Mulhaupt, R. W. James, A. E.I. Proudfoot, and F. Mach Antagonism of RANTES Receptors Reduces Atherosclerotic Plaque Formation in Mice Circ. Res., February 6, 2004; 94(2): 253 - 261. [Abstract] [Full Text] [PDF]
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A. Diez-Juan, P. Perez, M. Aracil, D. Sancho, A. Bernad, F. Sanchez-Madrid, and V. Andres Selective inactivation of p27Kip1 in hematopoietic progenitor cells increases neointimal macrophage proliferation and accelerates atherosclerosis Blood, January 1, 2004; 103(1): 158 - 161. [Abstract] [Full Text] [PDF]
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D. D. Wagner and P. C. Burger Platelets in Inflammation and Thrombosis Arterioscler Thromb Vasc Biol, December 1, 2003; 23(12): 2131 - 2137. [Abstract] [Full Text] [PDF]
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P. Ferroni, F. Martini, C. M. Cardarello, P. P. Gazzaniga, G. Davi, and S. Basili Enhanced Interleukin-1{beta} in Hypercholesterolemia: Effects of Simvastatin and Low-Dose Aspirin Circulation, October 7, 2003; 108(14): 1673 - 1675. [Abstract] [Full Text] [PDF]
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B. OSTERUD and E. BJORKLID Role of Monocytes in Atherogenesis Physiol Rev, October 1, 2003; 83(4): 1069 - 1112. [Abstract] [Full Text] [PDF]
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H. Koyama, T. Maeno, S. Fukumoto, T. Shoji, T. Yamane, H. Yokoyama, M. Emoto, T. Shoji, H. Tahara, M. Inaba, et al. Platelet P-Selectin Expression Is Associated With Atherosclerotic Wall Thickness in Carotid Artery in Humans Circulation, August 5, 2003; 108(5): 524 - 529. [Abstract] [Full Text] [PDF]
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H.-J. Anders, M. Frink, Y. Linde, B. Banas, M. Wornle, C. D. Cohen, V. Vielhauer, P. J. Nelson, H.-J. Grone, and D. Schlondorff CC Chemokine Ligand 5/RANTES Chemokine Antagonists Aggravate Glomerulonephritis Despite Reduction of Glomerular Leukocyte Infiltration J. Immunol., June 1, 2003; 170(11): 5658 - 5666. [Abstract] [Full Text] [PDF]
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P. C. Burger and D. D. Wagner Platelet P-selectin facilitates atherosclerotic lesion development Blood, April 1, 2003; 101(7): 2661 - 2666. [Abstract] [Full Text] [PDF]
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 K. Nakajima, Y. Tanaka, T. Nomiyama, T. Ogihara, F. Ikeda, R. Kanno, N. Iwashita, K. Sakai, H. Watada, T. Onuma, et al. RANTES Promoter Genotype Is Associated With Diabetic Nephropathy in Type 2 Diabetic Subjects Diabetes Care, March 1, 2003; 26(3): 892 - 898. [Abstract] [Full Text] [PDF]
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A. Schober, D. Manka, P. von Hundelshausen, Y. Huo, P. Hanrath, I. J. Sarembock, K. Ley, and C. Weber Deposition of Platelet RANTES Triggering Monocyte Recruitment Requires P-Selectin and Is Involved in Neointima Formation After Arterial Injury Circulation, September 17, 2002; 106(12): 1523 - 1529. [Abstract] [Full Text] [PDF]
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 T. S. Olson and K. Ley Chemokines and chemokine receptors in leukocyte trafficking Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2002; 283(1): R7 - R28. [Abstract] [Full Text] [PDF]
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 P. AUKRUST, T. WAeHRE, J. K. DAMAS, L. GULLESTAD, and N. O. SOLUM Inflammatory role of platelets in acute coronary syndromes Heart, December 1, 2001; 86(6): 605 - 606. [Full Text] [PDF]
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P. Libby and D. I. Simon Inflammation and Thrombosis : The Clot Thickens Circulation, April 3, 2001; 103(13): 1718 - 1720. [Full Text] [PDF]
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