© 1995 American Heart Association, Inc.
Articles |
Adsorption and Coagulability of Fibrinogen on Atheromatous Lipid Surfaces
From the Department of Pathology and Laboratory Medicine, University of Cincinnati Medical Center, Cincinnati, Ohio.
Correspondence to Gregory S. Retzinger, MD, PhD, Department of Pathology and Laboratory Medicine, University of Cincinnati Medical Center, 231 Bethesda Ave, Cincinnati, OH 45267-0529.
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Abstract |
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Abstract Fibrinogen, the precursor of the blood clot matrix and a major constituent of atherosclerotic lesions, is shown to adsorb with high affinity to hydrophobic beads coated with cholesteryl oleate, cholesterol, or loosely packed lecithin. The quantity of fibrinogen that binds to cholesterol- or lecithin-coated beads decreases as the surface concentration of the lipid increases; densely packed films of lecithin bind little, if any, of the protein. In sharp contrast, the appreciable quantity of fibrinogen that binds to cholesteryl oleate–coated beads is indifferent to the surface concentration of that lipid. Not unexpectedly, the quantity of fibrinogen that binds to beads coated with mixtures of cholesteryl oleate and lecithin increases with increasing concentration of the cholesteryl ester. When bound, fibrinogen can be converted by thrombin to fibrin and nucleate clot formation as manifested by the aggregation of stirred beads. These results indicate that hydrophobic, atheromatous lipid surfaces, particularly those rich in cholesteryl esters, may be predisposed to thrombosis by virtue of their inherent capacity to bind functional fibrinogen.
Key Words: fibrinogen • lipid surfaces • atherosclerosis • thrombosis
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Introduction |
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Like cholesterol and its esters, fibrinogen, the precursor of the blood clot matrix, is a major component of atherosclerotic lesions, and the fibrinogen concentration of these lesions appears to correlate positively with their lipid content.1 2 3 4 Like cholesterol, fibrinogen is also a major risk factor for atherosclerosis.5 6 7 Indeed, most of the morbid and mortal consequences of atherosclerosis derive from fibrinogen-dependent thrombotic events intimately related to the development and growth within the arterial wall of lipid deposits, ie, plaques, that are rich in cholesterol and cholesteryl esters.8 Importantly, therapies mitigating the effects of atherosclerosis most frequently include anticoagulation. Thus, the accumulation of fibrinogen on or about atherosclerotic lesions does not appear to be incidental and may, in fact, contribute to processes leading to plaque formation and progression.1 2 3 4 It would be worthwhile, therefore, to elucidate the mechanism by which fibrinogen becomes incorporated into the lipid-rich lesions that define atherosclerosis.
Evidence indicates that clots in vivo are initiated on newly formed surfaces, in part because fibrinogen accumulates on these surfaces.9 10 11 This last phenomenon is of particular interest to biomedical materials researchers who seek to understand the basis for the relatively selective uptake of fibrinogen by any synthetic, hydrophobic or amphiphilic surface in contact with blood. This interest is certainly warranted since, once bound from plasma,12 fibrinogen can nucleate clot formation, thus potentially leading to thrombosis and a host of biological processes attending thrombosis, including retraction of endothelial cells and recruitment and adhesion of platelets and inflammatory cells.13 14 15 16 Indeed, recognition of these potentialities has guided the formulation and screening of polymeric materials for use in circulatory prosthetics since materials that do not bind fibrinogen are, in general, considered "hemocompatible."17 18 19 20 But, as shown by the deposition on atherosclerotic lesions, fibrinogen deposition from blood is not unique to the surface of synthetic materials. Fibrinogen accumulates in vivo not only on or near atherosclerotic lesions but also on many other naturally occurring surfaces including the cytoplasmic membrane of certain cells,15 21 22 eg, platelets, macrophages, and tumor cells. While in most instances the binding of fibrinogen to cells appears to be mediated by specific proteins expressed on the outer surface of the cell membrane, the binding of fibrinogen to relatively acellular, hydrophobic sites, eg, atherosclerotic plaques, need not be mediated by such receptors. More likely, adsorption of fibrinogen to such sites is a consequence of physicochemical processes similar to those accounting for adsorption of the protein to the synthetic, hydrophobic materials used in the manufacture of circulatory prosthetics. These sites would then be subject to and participate in many of the fibrinogen-mediated processes that characterize the biological responses to the synthetic materials.
Since physicochemical properties of surfaces play such an important role in the adsorption of fibrinogen, it is not unreasonable to propose that molecular features dictating the capacity and affinity of some biological surfaces for fibrinogen derive from particular properties of lipids. Because not all lipid deposits are atheromatous and bind fibrinogen, something peculiar to the lipid of atherosclerotic lesions must confer on these lesions their capacity for this adhesive protein. Consistent with the observed affinity of synthetic, hydrophobic materials for fibrinogen, this "peculiarity" might derive from the hydrophobicity of cholesteryl esters, the major lipids of atherosclerotic lesions.23
A rigorous test of such a proposal might involve the formulation and use of well-defined lipid surfaces. Such well-defined lipid surfaces have already been prepared and characterized; they simply involve coating microscopic, polystyrene-divinylbenzene beads with lipids.24 25 These beads can then be used advantageously to assess the influence of the lipid microenvironment on the adsorption and subsequent polymerization and proteolyis of fibrin(ogen).26 27 28 29 This article reports on the use of hydrophobic beads for exploring the interactions of fibrinogen with lecithin-, cholesterol-, and/or cholesteryl oleate–coated surfaces. The data indicate that the identity and/or packing density of the lipid influences the adsorption of fibrinogen to the coated surface. In particular, surfaces coated with cholesteryl oleate adsorb fibrinogen avidly, even from plasma. As a consequence of this adsorption, such surfaces should be expected to function as clot nucleation sites and thus influence a host of fibrin(ogen)-mediated processes.
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Methods |
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Reagents and Chemicals
Human fibrinogen, grade L, from Kabi AB was dialyzed exhaustively against deionized water, divided into aliquots, and stored at -20°C until use. According to the manufacturer, this commercial fibrinogen contains only trace amounts of factor XIII and no more than 0.9% by weight of plasmin(ogen)-related materials. Before use, a frozen aliquot of fibrinogen solution was first thawed to room temperature, diluted to a desired concentration by using an appropriate buffered salt solution, and then heated to 37°C to dissolve any residual cryoprecipitate. The fibrinogen concentration of stock solutions was determined by using the molar absorptivity of the protein at 280 nm, 5.12x105 L · mol-1 · cm-1.30 Fibrinogen was uniformly labeled by using Na125I from Amersham and Iodo-Gen from Pierce.31 Fatty acid–free bovine serum albumin was from Miles Biochemicals. Egg yolk L-
-lecithin from Avanti Polar Lipids was dissolved in
absolute ethanol and stored under nitrogen at -20°C until use. This
lecithin (Mr, 786) contains predominantly
C16 and C18 fatty acid esters, of which
approximately half are monounsaturated or diunsaturated. Cholesteryl
oleate and anhydrous cholesterol were from Sigma.
1-Palmitoyl-2-[1-14C]oleoyl-L-3-phosphatidylcholine
(specific activity, 2.11 GBq/mmol), [14C]cholesterol
(2.16 GBq/mmol), and [1,2(n)-3H]cholesteryl oleate
(1.67 TBq/mmol) were from Amersham. Human thrombin (>3000 U/mg) was
from Sigma. Polystyrene-divinylbenzene beads of 6.4±1.9 µm diameter
and beads of 0.945±0.0064 µm diameter were from Seragen Diagnostics.
Prior to coating with lipids and/or fibrinogen, the larger beads were
washed.24 Water was deionized and then distilled by using
an all-glass apparatus. Organic solvents were of a grade suitable for
high-performance liquid chromatography. All other chemicals were of the
highest quality available commercially. Fresh plasma was prepared from
the blood of a healthy donor known to have a "low normal" plasma
concentration of fibrinogen. For this purpose, blood was drawn directly
into evacuated siliconized glass tubes containing sodium citrate,
yielding a final concentration of the anticoagulant of 0.013 mol/L
(Becton Dickinson). Blood cells were pelleted by centrifugation at
1500g for 10 minutes, and the citrated plasma was then
aspirated into plastic tubes and stored at -20°C until use.
Coating Beads With Lipids and/or Fibrinogen
Beads were first washed and lyophilized.24 Beads
(up to 350 mg) were placed in a glass tube containing the desired
lipid(s) in 3.0 mL hexane/ethanol (9:1, vol/vol). The beads were
dispersed briefly by using an ultrasonic water bath and then dried with
a stream of nitrogen. The dry beads were redispersed in 3.0 mL
glass-distilled water, pelleted by centrifugation at 300g
for 3 minutes, washed twice with 3.0 mL water, and used immediately
after dispersion in 0.02 mol/L Tris-HCl, pH 7.40, containing 0.15 mol/L
KCl. Radiolabeled lipids were used to determine the amount of lipid
that bound to a known amount of beads.25
Adsorption isotherms of 125I-fibrinogen were generated by using both uncoated and lipid-coated beads.25 In brief, beads were dispersed in 0.02 mol/L Tris-HCl, pH 7.40, containing 0.15 mol/L KCl and a predetermined concentration of 125I-fibrinogen. The radioactivity bound to the beads was then determined. The final bead concentration of the fibrinogen binding assays was 6.7 mg/mL.
Thrombin-Inducible Aggregation of Beads as a Measure of the
Functionality of Bound Fibrinogen
When stirred in the presence of thrombin, beads coated with an
appropriate layer of fibrinogen aggregate as a consequence of interbead
fibrin formation, and thus, thrombin-inducible aggregation is a
convenient measure of the functionality of the bead-bound fibrinogen.
While thrombin quantitatively liberates both fibrinopeptides A and B
from fibrinogen adsorbed to beads, the liberation of fibrinopeptide A
alone is necessary and sufficient for bead aggregation to
occur.32 A detailed description of the aggregation assay
is available.32 When using an aggregometer, a typical
aggregation assay is performed at room temperature as follows. A 0.5-mL
dispersion containing 0.02 mol/L Tris-HCl, pH 7.40, 1.0 mg/mL bovine
serum albumin, and 1.0 mg/mL beads, ie, 
8.07x106
beads/mL, is added to the cylindrical, glass sample cuvette (internal
diameter, 6 mm). This dispersion has an apparent absorbance of 1.0 at
500 nm when a 1.0-cm path length cuvette is used. As reference
material, a dispersion of beads of diameter 0.945±0.0064 µm is
routinely used. The apparent absorbance of this reference dispersion is
0.5 at 500 nm when using a cuvette of 1.0-cm path length. Once the
baseline signal of the stirred (1000 rpm) test sample is established,
20 µL of an aqueous solution containing 0.5 NIH U of human thrombin
is added to the reaction cuvette. The relative absorbance of the sample
as a function of time is then recorded. A value of 1.0 is arbitrarily
assigned to the maximal change of the aggregometry signal that occurs
after the addition of 0.5 U thrombin to beads coated with a mixed film
of lecithin (0.08 µg/cm2) and fibrinogen (0.38
µg/cm2). When measured at 500 nm by using a
spectrophotometer and a 1.0-cm cuvette, this change in apparent
absorbance corresponds to 0.85 absorbance unit.
Removal and Analysis of Proteins From Beads
Proteins were eluted from beads by using an aqueous solution
containing sodium dodecyl sulfate (SDS; 4%, wt/vol) and, as necessary,
2-mercaptoethanol (5%, vol/vol).12 These polypeptides
were then separated by using polyacrylamide gel electrophoresis in the
presence of SDS.33 The stacking gel was 4% polyacrylamide
and the resolving gel, 10% polyacrylamide. Prior to electrophoresis,
samples were diluted with an equal volume of 0.125 mol/L Tris-HCl, pH
6.80, and glycerol 20% (vol/vol). They were then heated to 80°C for
10 minutes. Materials eluted from beads were either stained in gels
directly by using a commercial silver stain (Pierce) or
electrophoretically transferred to polyvinylidene difluoride membranes
for limited N-terminal sequence analysis and/or amino acid
analysis by personnel of the Protein and Nucleic Acid Shared
Facility of the Medical College of Wisconsin. The identities of
sequences were determined by using a computer-facilitated search of the
most recent update of the Protein Sequence Database of the Protein
Identification Resource, the National Biomedical Research Foundation,
Washington, DC.
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Results |
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Adsorption of Fibrinogen to Lipid-Coated Beads
Once coated onto polystyrene-divinylbenzene beads, lecithin, cholesterol, and/or cholesteryl oleate remain associated with the beads even if the coated beads are stored in citrated plasma for more than 2 weeks. Binding of fibrinogen to beads coated with any of the lipids is a saturable process27 29 32 (Fig 1
). As is
generally true for the adsorption of proteins onto hydrophobic
surfaces,9 10 11 the adsorption of fibrinogen onto beads
coated with any of the lipids of this study is irreversible and thus
precludes rigorous analysis of the binding data according to a
conventional equilibrium scheme. The saturation value, however, does
provide an excellent estimate of the capacity of the lipid-coated beads
for the protein. Additionally, because desorption is so slow, the
surface concentration of fibrinogen remains essentially constant during
the course of most experiments, and, consequently, these beads can be
used to assess the role(s) of the bound lipid on both adsorption and
proteolysis of the protein.26 27 28 29
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The adsorption of fibrinogen to beads coated with either lecithin or
cholesterol decreases in linear fashion with increasing lipid
concentration (Fig 2). The minimum amount of fibrinogen
bound to these beads approaches but does not reach zero. Instead, the
profiles become discontinuous at 0.16 and 0.21
molecule/Å2 for lecithin and cholesterol, respectively,
indicating that a constant amount of protein binds to the otherwise
hydrophobic surface once the limiting area of these lipids is
reached.34 The minimum, nominal surface concentration of
fibrinogen on cholesterol-coated beads is 0.25
µg/cm2, or about tenfold higher than that of
lecithin-coated beads. From these data, it can be inferred that the
binding capacity of the otherwise hydrophobic surface of the bead is
reduced by an amount proportional to the area occupied by the
hydrophilic head group of the adsorbed lipid. As the area per lipid
approaches that of the head group, which does not bind protein, the
capacity of the surface for the protein is reduced accordingly. In the
case of lecithin, which is more compressible than
cholesterol,34 the limiting area is approximately
equivalent to that of the choline head group. Thus, at high coverage of
the surface by lecithin, little protein binds. As determined by using
Corey-Pauling-Kolton space-filling models, the lone hydroxyl of
cholesterol, however, accounts for no more than 50% of the limiting
area of the molecule. Thus, even at high surface coverage by
cholesterol, appreciable hydrophobic space will be available for
protein adsorption. Beads coated with cholesteryl oleate are distinctly
different from those coated with either lecithin or cholesterol in that
binding of fibrinogen to these beads is independent of the surface
concentration of the lipid. Such a result reflects the absence of
a hydrophilic function of the cholesteryl ester. A diagrammatic
representation of the hypothetical condition existing on the
surface of beads coated maximally with the individual lipids is given
in Fig 3.
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), cholesterol (
), or cholesteryl oleate
(
). The initial concentration of fibrinogen in solution was
7.40x10-7 mol/L, a concentration that ensures saturation
of the lipid-coated surface given the conditions of the binding
assay.
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Removal and Identification of Proteins Adsorbed to Lipid-Coated
Beads
An aqueous solution of SDS and 2-mercaptoethanol elutes proteins
from both unmodified and lipid-coated beads.12 Significant
differences in the capacities of the various lipid-coated beads for
fibrinogen are obvious from silver-stained gels containing materials
eluted from the beads after their exposure to buffer containing
fibrinogen alone as protein (Fig 4A). These same
differences are observed for plasma proteins in general if beads coated
with the individual lipids are exposed to citrated plasma (Fig 4B). As
expected,9 10 11 12 despite the low normal concentration of
fibrinogen in this plasma, that protein is still the dominant protein
of those in the adsorbed film. Albumin and immunoglobulin are also
represented in these adsorbed films.12 An as
yet unidentified material of Mr >94 000
(probably close to Mr 150 000) is
conspicuous in the eluate from cholesterol-coated beads but is only
barely visible in the eluates from beads coated with the other two
lipids individually. A limited, N-terminal sequence of this
material12 has no significant homology with any
polypeptide now catalogued in the Protein Identification Resource.
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-chain. B, Lipid-coated beads (20 mg) were
dispersed in 4.0 mL citrated plasma obtained from a healthy donor and
then incubated in this medium for an additional 20 minutes. The
fibrinogen concentration of this plasma was
Thrombin-Inducible Aggregation of Lipid-Coated Beads That Bind
Fibrinogen
In addition to yielding valuable quantitative information on the
binding of fibrinogen to lipid films, the bead system can be used to
assess rapidly and conveniently the coagulability of the adsorbed
fibrinogen. In the presence of thrombin or enzymes of thrombin-like
specificity, beads coated with a monolayer of fibrinogen aggregate when
stirred in an aqueous phase, a consequence of interbead fibrin
dimerization.32 This aggregation can be monitored
turbidimetrically by using a platelet aggregometer or even a
spectrophotometer equipped with a stirred cell. The decrease in
absorbance that follows the addition of thrombin to a stirred
dispersion of fibrinogen-coated beads corresponds to the formation of
bead aggregates of increasing size (Fig 5). The maximal
slope of the tracing, ie, the maximal rate of aggregation, is
proportional to thrombin activity and can be used to quantify the
enzyme.32 For a fixed amount of thrombin, the rate and
extent of aggregation depend on the concentration of adsorbed
fibrinogen.
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The rate of aggregation of beads that are coated with the various
lipids and then exposed to fibrinogen reflects the capacity of the
lipid-coated particles for the protein (Figs 2
and 6).
Beads coated with a liquid-expanded film of lecithin (160
Å2/molecule) or even a condensed film of
cholesterol or cholesteryl oleate all bind 
0.25 µg/cm2
fibrinogen and, consequently, aggregate when stirred in the presence of
thrombin. In marked contrast, beads coated with a membrane-mimetic,
condensed film of lecithin bind almost no fibrinogen and do not
aggregate when stirred in the presence of thrombin. With the notable
exception of beads coated with a condensed film of cholesterol, these
same tendencies are observed when citrated plasma is used as the
coating medium instead of buffered fibrinogen (Fig 6B). The
inability of cholesterol-coated beads to aggregate after exposure
to plasma and then thrombin may be a consequence of these beads having
bound insufficient fibrinogen to stabilize developing bead aggregates
under the conditions of the turbidimetric assay. This reduced capacity
for fibrinogen may, in turn, be a consequence of occupancy of the
cholesterol-coated surface by the unidentified polypeptide of apparent
Mr >94 000 (Fig 4).
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Mixed Films of Lecithin and Cholesteryl Oleate
Having delineated the relations between fibrinogen binding and the
surface concentration of lecithin, cholesterol, and cholesteryl oleate
bound individually to beads, an assessment was next made of the
adsorption of fibrinogen to surfaces coated with mixed films of
lecithin and cholesteryl oleate, since such films would more closely
mimic the lipid composition of an atherosclerotic
lesion.23 The amount of fibrinogen that binds to a surface
coated with these mixed films is a function of both the lipid packing
density and, for a given packing density, the ratio of the two lipids
(Fig 7). Increasing the cholesteryl ester content
increased the capacity of the surface for fibrinogen. This increasing
capacity for fibrinogen was reflected, again, in the thrombin-induced
aggregability of the particles (Fig 8).
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Discussion |
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Taken together, these results argue that the capacity of a lipid surface for binding fibrinogen and, consequently, the thrombogenic potential of the surface depend on the availability of hydrophobic domains exposed at the interface: lipid surfaces with appreciable hydrophobic character will bind fibrinogen and, because of this binding, will be thrombogenic. This principle is relevant, mechanistically, to a host of disease processes that involve lipid surfaces and thrombosis, an important example of which is atherosclerosis. Atherosclerotic lesions are rich in fibrin(ogen) and both intracellular and extracellular lipids.1 2 3 4 23 Of these lipids, cholesteryl esters are the most conspicuous, accounting for as much as 80% to 90% of the lipid of atherosclerotic lesions most associated with overt thrombosis, ie, advanced plaques.23 Given the results presented here, it is reasonable to assume that the high affinity of cholesteryl ester–rich surfaces for fibrinogen accounts in part for the thrombotic predisposition of atherosclerotic lesions, and measures that reduce either fibrinogen concentration or the capacity of the lesions for the protein should reduce this predisposition. Such notions are eminently consistent with current opinions on the importance of both cholesterol/cholesteryl esters and fibrinogen in atherosclerosis1 2 3 4 5 6 7 8 and, in fact, provide a rationale unifying these opinions.
While this work relates to the interactions of fibrinogen with deposits of extracellular lipid, it may also relate to the interactions of fibrinogen with living cells. It is tempting to speculate that, in certain instances, the deposition/adsorption of fibrinogen onto cells, including platelets, macrophages, tumor cells, and erythrocytes,35 is driven by membrane alterations that yield hydrophobic patches on the surface of these cells. Such alterations might include redistribution36 37 38 or chemical modification39 40 of existing membrane lipids or a change in membrane lipid composition.41 42 Having bound fibrinogen, these cells would then be primed to participate in all the processes involving the protein, including adhesion, inflammation,43 metastasis,44 45 and thrombosis.
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Acknowledgments |
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This work was supported by a grant from the Lucille P. Markey Charitable Trust; the author is a Lucille P. Markey Scholar. He thanks Ruth Mary Retzinger for inspiration.
Received October 26, 1994; accepted March 16, 1995.
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