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Prepublished online as a Blood First Edition Paper on July 5, 2002; DOI 10.1182/blood-2002-03-0712.
RED CELLS
From the Department of Chemical Engineering, Institute
for Medicine and Engineering, University of Pennsylvania, Philadelphia.
Deep vein thrombosis (DVT) is a low flow pathology often prevented
by vascular compression to increase blood movement. We report new
heterotypic adhesive interactions of normal erythrocytes operative at
low wall shear rates ( Adhesion of erythrocytes to the blood vessel wall
is of considerable significance in pathologies involving vasoocclusive
events such as sickle cell anemia. Most previous studies on adhesive interactions of erythrocytes have been targeted toward sickle red blood
cells or plasmodium falciparum-infected erythrocytes. Some of the
molecules mediating sickle red cell adhesion to the endothelium are
P-selectin,1 thrombospondin (TSP),2,3 von
Willebrand factor (VWF),4 CD36,3,5 sulfated
glycolipid,6 Platelets adhere to the blood vessel wall through interactions mediated
by glycoproteins, GP Ia/IIa, GP IIb/IIIa, and GP Ib-IX, which bind
primarily to collagen,13 fibrinogen,14 and
VWF,15 respectively, on the vessel wall surface.
Similarly, the capture of neutrophils to the vessel wall involves
neutrophil P-selectin glycoprotein ligand 1 (PSGL-1)-mediated
rolling16 and membrane tethering17 on
P-selectin presented by activated endothelium or spread
platelets,18 followed by
TSP, a complex trimeric glycoprotein, can interact with platelets
through multiple adhesive molecules and receptors such as collagen,
laminin, fibronectin, fibrinogen,23 sulfated
glycolipids,24 VWF,25 CD36, and
possibly GPIa/IIa.26 TSP may promote platelet aggregation
by crossbridging platelet-bound fibrinogen.27 TSP, abundant in clots28 and uncrosslinked
fibrin,29 may accelerate fiber growth during fibrin
polymerization.28 Additionally, a role for TSP in adhesion
of neutrophils to the vessel wall has also been
suggested.30,31
The objective of this study was to examine capture and adhesion of
normal erythrocytes to surface-adherent neutrophils and platelets under
low flow conditions as a mechanism of red blood cell (RBC) accumulation
distinct from passive entrapment within fibrin fibers. We hypothesized
that red blood cells could adhere to activated neutrophils, activated
platelets, and surface-deposited fibrin under venous flow conditions
through receptor-mediated adhesion. This hypothesis is motivated by the
observation that deep vein thrombosis (DVT) is a pathology associated
with depressed shear rates and is significantly prevented in high-risk
postsurgical patients by vascular compression to prevent stasis.
However, it is unclear how depressed flow serves as a causative agent
or predisposing factor during DVT. Our studies support a role for
inflammation causing neutrophil or platelet arrest and activation on
activated endothelium with subsequent receptor-mediated capture of red
blood cells (or rouloux) under low flow conditions to help precipitate DVT.
Materials
Cell isolation
Microcapillary flow chambers Rectangular glass capillaries (Vitrocom, Mountain Lakes, NJ) with a cross section of 0.2 × 2.0 mm, a length of 7 cm, and a wall thickness of 0.15 mm were used as flow chambers as previously described.17,32 To enable adhesion of neutrophils or platelets, microcapillary flow chambers were incubated with human fibrinogen solution (100 µg/mL) for 120 minutes at room temperature or with calf skin collagen (100 µg/mL) for 4 hours at 4°C. The chambers were rinsed and cells were allowed to adhere under no-flow conditions as described previously.32 In some experiments, adherent platelets were treated with anti-GPIIb (25 µg/mL), anti-GPIb (25 µg/mL), anti-P-selectin (25 µg/mL), anti-CD36 (25 µg/mL), anti-VWF (1:40 dilution), polyclonal anti-TSP (1:40 dilution), anti- v (25 µg/mL), anti- 1 (25 µg/mL),
anti-CD47 (25 µg/mL), anti-TSP A4.1 (25 µg/mL), or anti-TSP C6.7
(25 µg/mL) for 20 minutes. While anti-TSP A4.1 was used to inhibit
the binding of TSP to CD36, anti-TSP C6.7 was used to block binding of
the cell/platelet binding domain (CBD) through which TSP interacts with
CD47/IAP.33 In some experiments, adherent neutrophils were
treated with anti-CD36 or anti-TSP. In selected experiments, a purified
fibrin surface was formed by incubation of the chamber with thrombin
(10 U/mL) for 2 hours at room temperature, followed by perfusion of
fibrinogen solution (3 mg/mL) through the chamber for 10 minutes at 100 s 1 to form an observable fibrin layer. In some
experiments, human TSP (25 µg/mL) was perfused over a purified fibrin
surface for 20 minutes at 50 s1.
Perfusion of erythrocytes and digital imaging Erythrocytes were perfused into the flow chambers containing defined surface compositions at a controlled flow rate using a syringe pump (Harvard Apparatus, Holliston, MA). The wall shear stress ( w) imposed on the surface was calculated from the
solution of the Navier-Stokes equation for laminar flow of a Newtonian fluid: w = (6Qµ)/(B2W), where Q
represents the flow rate (cm3/s), µ represents the
viscosity (0.01 Poise at room temperature), B represents the total
plate separation (0.02 cm), and W represents the width (0.2 cm).
Consequently, the wall shear rate,  w (s1),
can be calculated as w = 6Q/B2W. Flow
rates of 20, 40, 60, and 80 µL/min corresponded to shear stresses of
0.25, 0.50, 0.75, and 1.00 dyne/cm2 and wall shear rates of
25 s1, 50 s1, 75 s1, and 100 s1. In some experiments, the red cells were preincubated
with anti-GPIIb (25 µg/mL), anti-GPIb (25 µg/mL), anti-P-selectin
(25 µg/mL), anti-CD36 (25 µg/mL), anti-CD18 (25 µg/mL), anti-VWF
(1:40 dilution), polyclonal anti-TSP (1:40 dilution), anti-TSP A4.1
(25 µg/mL), or anti-TSP C6.7 (25 µg/mL) for 20 minutes prior to
perfusion. In other experiments, red cells were incubated with
anti-CD11a (60 µg/mL), anti-CD11b (60 µg/mL), anti-CD11c (60 µg/mL), anti-v (25 µg/mL), anti-1 (25 µg/mL), anti-CD47 (25 µg/mL), or anti-LW (1:5 dilution) for the
same duration. To activate surface-adherent neutrophils in the flow
chamber, 20 µM fMLP was added to the erythrocytes before perfusion.
To activate fibrinogen-adherent platelets, either convulxin (10 nM) or
thrombin (1 U/mL) was added to the red cells prior to their perfusion
over platelets. During flow experiments, the microcapillary flow
chambers were mounted on a Zeiss Axiovert 135 microscope (Thornwood,
NY), and a 63X (NA 1.40) oil immersion objective lens (Plan Apochromat)
was used to conduct differential interference contrast (DIC)
microscopy. An Argus 20 image processor (Hamamatsu, Bridgewater, NJ)
was used for contrast enhancement and real-time frame averaging. Images
were acquired using a closed-circuit digital (CCD) camera (Hamamatsu)
or a high-speed digital camera (MotionCorder Analyzer; Eastman Kodak,
New York, NY) and were recorded on videotape. Following image
acquisition, adherent cells were counted for multiple fields of view
(n > 15) to calculate the cell adherence per unit area or the cell
adherence per 100 neutrophils.
Adhesion of erythrocytes to platelets Washed erythrocytes were perfused over collagen-adherent platelets atw = 50 s1 for 5 minutes to
investigate the interactions between erythrocytes and platelets under
flow. Many events of red cell capture, transient tethering, and/or firm
adhesion to platelets were observed (Figure 1A). In a typical short-lived event,
following capture, tethering, and a pause for 400 ms, an adherent red
cell was released by the platelet. Of the total adhesion events
observed between erythrocytes and collagen-adherent platelets in 5 separate flow chambers during a perfusion period of 5 minutes for each
chamber, 46% of the cells remained adherent for over 50 seconds, and
about 67% remained adherent for over 10 seconds. Only about 18% were
detached within one second, a time more characteristic of low bond
numbers.
To examine the dependence of erythrocyte adhesion on platelet
activation, erythrocyte adhesion on collagen-adherent platelets was
compared to that over fibrinogen-adherent platelets. Red cells were
perfused over fibrinogen-adherent platelets (Figure 1B) and collagen-adherent platelets (Figure 1C) in separate flow chambers at
To confirm that adhesive interactions of erythrocytes with platelets
are activation state-dependent, washed erythrocytes were perfused with
the glycoprotein VI (GPVI)-agonist36,37 convulxin (10 nM) over fibrinogen-adherent platelets at To investigate the role of P-selectin, CD36, GPIb, GP IIb/IIIa, TSP, or
VWF in erythrocyte adhesion to collagen-adherent platelets, red cells
were treated with blocking antibodies and perfused over platelets also
pretreated with the same antibody. In 5 separate experiments with a
polyclonal antibody against TSP and an antibody specifically directed
toward blocking the interaction of TSP with CD36, no reduction in RBC
adhesion to collagen-adherent platelets was found (Figure 2A).
Similarly, antibodies against GPIIb, VWF, and P-selectin had no effect.
Treatment with anti-CD36 or anti-GPIb showed statistically significant
reduction (approximately 40%) in red cell adhesion (Figure 2A),
indicating a role for CD36 and GPIb in the process. Blocking antibodies
against When red blood cells containing K3-EDTA (4 mM) were
perfused over collagen-adherent platelets, adhesion was completely
blocked (100%), indicating the Ca++ or Mg2+
dependence of this process. Moreover, when erythrocytes containing EGTA (4 mM), supplemented with Mg2+ (2 mM), were
perfused over collagen-adherent platelets, adhesion was significantly
blocked (70%), indicating the Ca++-dependence of red cell
adhesive interactions with platelets. In experiments at
Adhesion of erythrocytes to neutrophils Washed red cells were perfused over fibrinogen-adherent neutrophils at a wall shear rate of 50 s1 for 5 minutes.
A few transient adhesion events were observed between red cells and
fibrinogen-adherent neutrophils. However, when neutrophils were
activated with 20 µM fMLP (added to the erythrocytes before
perfusion), the number of pausing events and firmly adherent red cells
to these activated neutrophils dramatically increased. Figure
3A shows a capture/membrane tethering
event lasting 800 milliseconds between an erythrocyte and an
fMLP-activated neutrophil. Out of the total adhesion events observed
between erythrocytes and fMLP-activated neutrophils in 4 separate flow chambers during a perfusion period of 5 minutes for each, 57% of the
cells remained adherent for over 50 seconds, 66% remained adherent for
over 10 seconds, and approximately 22% were detached within one
second.
A comparison between Figure 3B and Figure 3C shows that the extent of
red cell adhesion to activated neutrophils was considerably greater
than that to normal neutrophils. fMLP caused a 6-fold increase
(P < .005, n = 3) in RBC adhesion to neutrophils (67 RBC/100 neutrophils vs 11 RBC/100 neutrophils; Figure
4A). Also, RBC adhesion to fMLP-treated
neutrophils was significantly reduced as
The presence of anti-CD18 antibody significantly blocked adhesive
interactions between red cells and fMLP-activated neutrophils by 80%
(P < .005, n = 3; Figure 4C). Having observed the role of anti-CD18 in blocking adhesion, blocking antibodies against CD11a,
CD11b, or CD11c were used to specify if the neutrophil receptor
responsible for these interactions was LFA-1 (CD11a/CD18), Mac-1
(CD11b/CD18), or p150,95 (CD11c/CD18). Whereas antibodies against CD11a
or CD11c had no effect on adhesion (data not shown), anti-CD11b blocked
adhesion by 76% (P < .005, n = 4; Figure 4C) demonstrating that Mac-1 is the major mediator of adhesion on the
neutrophil. When red blood cells in anti-CD36 or anti-TSP were perfused
over fMLP-treated neutrophils also pretreated with the same antibody,
no significant reduction in adhesion was observed. When erythrocytes in
anti-LW were perfused over fMLP-activated neutrophils, a 40% reduction
(P < .01, n = 6; Figure 4C) in red cell adhesion to
neutrophils was observed. In contrast, antibodies directed toward
Adhesion of erythrocytes to fibrin To investigate possible adhesive interactions (not entrapment) between erythrocytes and fibrin, washed erythrocytes were perfused at 50 s1 over preformed fibrin fibers polymerized from
recalcified PFP. At t = 5 minutes, some RBC adhesion was observed
(Figure 5A). In order to determine if
this observed adhesion was a result of direct adhesive interaction
between fibrin and the red cell, washed erythrocytes were perfused over
fibrin fibers made from purified fibrinogen. Absence of adhesion to
purified fibrin (Figure 5B) demonstrated that the interaction was not
direct, but mediated by a molecule in plasma bound to fibrin. As TSP is
a plasma protein that can mediate multiple interactions, we analyzed
its role by perfusing red cells over a purified fibrin surface treated
with TSP. The observed red cell adhesion to this surface (Figure 5C) indicated the role of TSP in mediating this interaction. However, this
role of TSP could not be verified because anti-TSP A4.1 did not show
any effect on RBC adhesion to fibrin from platelet-free plasma (PFP;
data not shown). Finally, the dependence of adhesive interactions
between erythrocytes and fibrin (from PFP) on divalent cations and
their fibrinogen sensitivity were tested for comparison to interactions
with platelets and neutrophils. Like adhesion to platelets, RBC
adhesion to fibrin from PFP was antagonized by soluble fibrinogen (3 mg/mL; Figure 5D) and was EDTA-sensitive.
Finally, to mimic pathophysiologic conditions more closely in the
presence of soluble fibrinogen and limited contact pathway activation,
PFP containing red blood cells, CTI (to inhibit Factor XIIa of the
contact pathway of coagulation32,38), and fMLP was perfused
at
We report that adhesion of normal erythrocytes to platelets at
depressed venous shear rates below 100 s Because platelet receptor GPVI mediates the adhesion and signaling responses to collagen37,39 and convulxin is a GPVI selective agonist,36,37,39 our results indicate that platelet GPVI is triggering signaling that leads to the adhesive interactions of erythrocytes with platelets. In addition to being EDTA-sensitive, the interaction was found to be ethyleneglycotetraacetic acid (EGTA)-sensitive (70% block), demonstrating the Ca++ dependence of the adhesive interactions between erythrocytes and platelets. As GPVI-mediated platelet activation occurs through Ca++-dependent pathways,39 the Ca++ dependence of erythrocyte-platelet adhesion events may involve GPVI signaling in mediating these interactions. Using a Dacron graft thrombosis model, Palabrica et al40 observed that anti-P-selectin inhibited neutrophil and fibrin accumulation as well as reduced RBC adhesion to the clot surface by an unknown mechanism. This decrease in red cells observed by Palabrica et al may be explained by adhesive mechanisms described in the present study. Although P-selectin may not have been directly involved in normal red cell adhesion, the reduction in fibrin and number of neutrophils in the clot may have led to diminished erythrocyte adhesion in the harvested grafts examined by Palabrica et al.40 Recent studies have suggested a role for adherent neutrophils in sickle
cell vascular occlusion.41 The initiation and propagation of vaso-occlusive processes in sickle disease has been associated with
neutrophil activation.42 We believe that adhesive
interactions of normal erythrocytes with adherent activated
neutrophils, like the ones we have presented in this study, can also
lead to vaso-occlusion under low shear rates (< 100 s Although it is known that vascular compression devices help
prevent DVT, the molecular mechanisms by which they do so have been
unclear.46,47 Our observation that firm adhesion of red cells to platelets and neutrophils is efficient at shear rates below
100 s Although the adhesion of erythrocytes to activated platelets is GPVI-triggered and partly CD36-dependent and their adhesion to activated neutrophils is mediated by Mac-1 and LW, the mediator(s) for RBC-fibrin interaction remains unclear. Even though RBCs firmly adhered to a TSP-coated fibrin surface, a TSP antibody did not block adhesion to PFP fibrin. Because TSP is a complex molecule that interacts with cells through multiple pathways including fibrinogen cross-bridging,27 it may be difficult to antagonize its effects using an antibody. Why have normal RBC adhesion processes not been detected or described
previously? Prior studies of platelet, neutrophil, and sickle cell
adhesion have generally been conducted at
Submitted March 6, 2002; accepted June 26, 2002.
Prepublished online as Blood First Edition Paper, July 5, 2002; DOI 10.1182/blood-2002-03-0712.
Supported by a grant from the National Institutes of Health (NIH) RO1 HL 56621. S.L.D. is an Established Investigator of the National American Heart Association. M.S.G. is an NIH predoctoral fellow (T32 HL 07954-02).
The publication costs of this article were defrayed in part by page charge payment. Therefore, and solely to indicate this fact, this article is hereby marked "advertisement" in accordance with 18 U.S.C. section 1734.
Reprints: Scott L. Diamond, Institute for Medicine and Engineering, Department of Chemical Engineering, University of Pennsylvania, 1010 Vagelos Research Laboratories, 3340 Smith Walk, Philadelphia, PA 19104; e-mail: sld{at}seas.upenn.edu.
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 J.-P. Bin, A. Doctor, J. Lindner, E. M. Hendersen, D. E. Le, H. Leong-Poi, N. G. Fisher, J. Christiansen, and S. Kaul Effects of Nitroglycerin on Erythrocyte Rheology and Oxygen Unloading: Novel Role of S-Nitrosohemoglobin in Relieving Myocardial Ischemia Circulation, May 30, 2006; 113(21): 2502 - 2508. [Abstract] [Full Text] [PDF]
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 K. Ganguly, M. S. Goel, T. Krasik, K. Bdeir, S. L. Diamond, D. B. Cines, V. R. Muzykantov, and J.-C. Murciano Fibrin Affinity of Erythrocyte-Coupled Tissue-Type Plasminogen Activators Endures Hemodynamic Forces and Enhances Fibrinolysis in Vivo J. Pharmacol. Exp. Ther., March 1, 2006; 316(3): 1130 - 1136. [Abstract] [Full Text] [PDF]
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T. J. Mankelow, F. A. Spring, S. F. Parsons, R. L. Brady, N. Mohandas, J. A. Chasis, and D. J. Anstee Identification of critical amino-acid residues on the erythroid intercellular adhesion molecule-4 (ICAM-4) mediating adhesion to {alpha}V integrins Blood, February 15, 2004; 103(4): 1503 - 1508. [Abstract] [Full Text] [PDF]
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 M. S. Goel and Scott. L. Diamond Neutrophil Cathepsin G Promotes Prothrombinase and Fibrin Formation under Flow Conditions by Activating Fibrinogen-adherent Platelets J. Biol. Chem., March 7, 2003; 278(11): 9458 - 9463. [Abstract] [Full Text] [PDF]
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P. Hermand, P. Gane, M. Huet, V. Jallu, C. Kaplan, H. H. Sonneborn, J.-P. Cartron, and P. Bailly Red Cell ICAM-4 Is a Novel Ligand for Platelet-activated alpha IIbbeta 3 Integrin J. Biol. Chem., February 7, 2003; 278(7): 4892 - 4898. [Abstract] [Full Text] [PDF]
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Abstract
Introduction
1 dyne/cm2.