(Circulation. 2000;102:2165.)
© 2000 American Heart Association, Inc.
Brief Rapid Communications |
Direct Proinflammatory Effect of C-Reactive Protein on Human Endothelial Cells
From the Department of Cardiology (E.T.H.Y.), University of Texas–M.D. Anderson Cancer Center, Houston, Tex; Department of Internal Medicine (V.P., 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, Houston, Tex; and the Texas Heart Institute (V.P., J.T.W., E.T.H.Y.), St. Luke’s Episcopal Hospital, Houston, Tex.
Correspondence to Edward T.H. Yeh, MD, Department of Cardiology, 1515 Holcombe Blvd, Box 70, University of Texas–M.D. Anderson Cancer Center, Houston, TX 77030-4095.
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Abstract |
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Background—The acute-phase reactant C-reactive protein (CRP) is an important risk factor for coronary heart disease. However, the possible effects of CRP on vascular cells are not known.
Methods and Results—We tested the effects of CRP on expression of
adhesion molecules in both human umbilical vein and coronary
artery endothelial cells. Expression of vascular cell
adhesion molecule (VCAM-1), intercellular adhesion molecule (ICAM-1),
and E-selectin was assessed by flow cytometry. Incubation with
recombinant human CRP (10 µg/mL) for 24 hours induced an 
10-fold
increase in expression of ICAM-1 and a significant expression of
VCAM-1, whereas a 6-hour incubation induced significant E-selectin
expression. Adhesion molecule induction was similar to that observed in
endothelial cells activated with
interleukin-1ß. In coronary artery
endothelial cells, induction of ICAM-1 and VCAM-1 was
already present at 5 µg/mL and reached a maximum at 50 µg/mL,
at which point a substantial increase in expression of E-selectin was
also evident. The CRP effect was dependent on presence of human serum
in the culture medium, because no effect was seen in cells cultured
with serum-free medium. In contrast, interleukin-1ß was able to
induce adhesion molecule expression in the absence of human serum.
Conclusions—CRP induces adhesion molecule expression in human endothelial cells in the presence of serum. These findings support the hypothesis that CRP may play a direct role in promoting the inflammatory component of atherosclerosis and present a potential target for the treatment of atherosclerosis.
Key Words: cell adhesion molecules • endothelium • atherosclerosis
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Introduction |
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Inflammatory response plays an important role in the onset, development, and evolution of atherosclerotic lesions.1 2 3 Elevated serum levels of C-reactive protein (CRP) have been widely considered to be nonspecific but sensitive markers of the acute inflammatory response. A number of epidemiological studies have shown that the acute-phase reactant CRP is an important risk factor for atherosclerosis and coronary heart disease.4 Higher levels of serum CRP are also related to increased risk of coronary events in patients with stable5 and unstable6 angina. The basic mechanisms responsible for this association are not clear; CRP may be merely a marker of inflammation, with no specific role in the pathogenesis of atherosclerosis. However, although CRP is present in atherosclerotic lesions, no previously reported study has specifically assessed the possible effects of CRP on vascular cells. Thus, the aim of this study was to assess the possible effects of CRP on the expression of adhesion molecules by human endothelial cells.
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Methods |
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Materials
Experiments were performed on human umbilical vein endothelial cells (HUVECs, from Cascade Biology) and in human coronary artery endothelial cells (HCAECs, from Clonetics). Cells were grown in M199 medium with endothelial cell growth supplement, heparin, and 15% fetal bovine serum or human serum. Cells were used at passages 2 to 4.
Recombinant human CRP and highly purified CRP from human serum were purchased from Calbiochem. Purity of CRP preparations was confirmed by 12% SDS-PAGE; no contaminating proteins were detected by silver staining of overloaded gels. Interleukin-1ß (IL-1ß) was provided by RandD Systems (Minneapolis, Minn). Human serum and fetal bovine serum were purchased from Sigma.
Detection of Adhesion Molecules
Endothelial cells were incubated with human CRP
for the indicated time, and adhesion molecule expression was detected
by flow cytometry as previously described.7
The fluorescence intensity of 9000 cells for each sample was quantified by a fluorescence-activated cell sorter Calibur analyser (Becton Dickinson). Mean fluorescence intensity values were corrected for unspecific staining by subtracting the fluorescence of cells stained with the isotype antibody and were compared with the Kolmogorov-Smirnov statistics provided by Cellquest software. Cell viability was assessed by direct cell counting in a hemocytometer after staining with trypan blue.
Adhesion of the monocytoid cell line U937 to HUVECs was assessed according to a previously published protocol.8 Differences between groups were assessed by Mann-Whitney U test.
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Results |
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CRP Induces Expression of Adhesion Molecules
Unstimulated HUVECs expressed low levels of intercellular adhesion molecule (ICAM-1) but no vascular cell adhesion molecule (VCAM-1) or E-selectin (Figure 1
). Cell viability by
trypan blue exclusion was >95% in all experiments. Remarkably, HUVECs
cultured with recombinant CRP (10 µg/mL for 24 hours) showed an
10-fold increase in the mean fluorescent intensity of ICAM-1
(from 43 to 405 mean fluorescence intensity) and a significant
expression of VCAM-1 (from 0 at baseline to 31 mean
fluorescence intensity) (Figure 1A and 1C). The
induction of adhesion molecule expression was similar to that observed
with a 24-hour incubation with IL-1ß (10 ng/mL), a well-known
activator of endothelial cells (Figure 1B and 1D). Although no induction of E-selectin was
evident after 24-hour incubation with CRP (or with IL-1ß), a 6-hour
incubation with CRP 10 µg/mL or IL-1ß induced a similar E-selectin
expression (mean fluorescence intensity from 1 to 28, Figure 1E and 1F). The biological activity of recombinant CRP on
HUVECs could also be duplicated by highly purified CRP obtained from
human serum (data not shown). Furthermore, induction was limited to
ICAM-1, VCAM-1, and E-selectin, because the level of CD31, a marker of
endothelial cells, remained unchanged in the presence
of CRP (Figure 1G and 1H).
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The biological significance of the adhesion molecule expression was confirmed by the significant increase of adhesion of U937 cells to HUVECs treated with 10 µg/mL CRP for 24 hours (from 1.7±1.2 cells in a 20x magnification field to 6.8±3.1 cells, P=0.005, mean of 6 fields).
Dose Response of CRP Effects in HCAECs
To extend our observations from HUVECs to arterial
endothelial cells involved in the pathogenesis of
atherosclerosis, we performed a dose-response
experiment in cultured HCAECs. Unstimulated HCAECs express significant
levels of ICAM-1, no VCAM-1, and low levels of E-selectin. The
dose-response relationship for the effect of CRP on ICAM-1, VCAM-1, and
E-selectin expression in HCAECs is shown in Figure 2 (A through I). The effect of CRP on
ICAM-1 and VCAM-1 was already present at a concentration of 5
µg/mL and was maximal at 50 µg/mL, whereas an increase in
E-selectin expression was evident only at concentrations >10 µg/mL,
with a significant increase at 50 µg/mL. An increase of CRP
concentration up to 100 µg/mL resulted in only a modest increase in
induction of adhesion molecules.
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Proinflammatory Effect of CRP Is Dependent on Serum
The results described above were achieved in the presence of 15%
human serum. Intriguingly, HUVECs cultured in serum-free medium did not
respond to 100 µg/mL CRP (Figure 2L
, 2M, and 2N). This was not due to the inability of HUVECs to express
adhesion molecules in the absence of serum, because IL-1ß (10 ng/mL)
induced adhesion molecule expression under the same conditions (Figure 2L, 2M, and 2N). The effects of CRP on
endothelial cells did not depend on the presence of LDL
or lipoproteins in the serum, because a similar induction of adhesion
molecules was observed with lipoprotein-free human serum (data not
shown).
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Our study shows that CRP can induce adhesion molecule expression by human endothelial cells. CRP is an acute-phase reactant usually present in human serum with a concentration <1 µg/mL. However, CRP levels can increase up to 100 or even 500 times during acute inflammation. This staggering response is mainly regulated by proinflammatory cytokines, in particular IL-6, and is largely unaffected by anti-inflammatory drugs.
High levels of CRP are frequently observed in unstable angina and acute myocardial infarction.6 In patients with unstable angina, serum levels >3 µg/mL are associated with increased risk of coronary events, and the association is stronger for patients with serum levels >10 µg/mL.6 Subsequent large epidemiological studies have shown that even small increases in serum levels of CRP are associated with higher risk of atherosclerosis and ischemic heart disease in apparently healthy subjects.9 10 Similarly, in patients with stable angina, serum levels of CRP >3.6 µg/mL are associated with a 2-fold increase in the risk of coronary events.5
Although there is now strong evidence that serum CRP levels are an
independent risk factor for ischemic heart
disease,4 10 the mechanisms underlying this association
are not clear. Because inflammatory responses play an important role in
the development and evolution of atherosclerosis and
may contribute to its thrombotic complications, serum CRP may be merely
a marker of inflammatory response. Alternatively, CRP may have a direct
role in the pathogenesis of
atherosclerosis.4 11 Because of its
ligand-binding properties, CRP plays a part in innate immunity
(opsonization) and in the removal of membrane and nuclear material from
necrotic cells. CRP can also bind to complement factor C1q and factor H
and activate the classic pathway of complement
activation.12 In addition, recent studies13
have shown that CRP can bind to receptor FC
RI (with low affinity)
and FCRII (with high affinity) on leukocytes. Interestingly, CRP is
present in atherosclerotic plaques, where it may colocalize with
the terminal complement complex.14 CRP can also induce
tissue factor expression by human monocytes.15
We found that CRP, at concentrations 
5 µg/mL, has significant
proinflammatory effects in both umbilical vein and coronary
artery endothelial cells, inducing high levels of
expression of ICAM-1, VCAM-1, and E-selectin. These findings compare
well with the results of previous large prospective studies showing
increased risk of cardiac events in patients with angina in the upper
quintile of CRP concentrations (ie, >3.6 µg/mL).5
Similarly, in patients with unstable angina, high serum CRP levels at
discharge and high CRP levels during follow-up are associated with
increased risk of new coronary events, especially in patients
in the upper tertile of serum CRP levels (>8.6
µg/mL).16 Our results suggest that the proinflammatory
effects of CRP may contribute to the adverse outcome associated with
higher levels of this acute-phase reactant. The increased expression of
adhesion molecules in the vascular wall is an important factor in the
development of atherosclerosis and may enhance the
local inflammatory response within atherosclerotic plaques by
recruiting monocytes and lymphocytes.17 Lowering serum CRP
levels may have beneficial effects on the evolution of
atherosclerosis and may reduce the risk of
coronary events. In a recent trial, long-term treatment with
statins was associated with a reduction in serum CRP levels and in
better clinical outcome after acute myocardial
infarction.18
The mechanisms of the proinflammatory effects of CRP on
endothelial cells are not completely clear. Indeed,
HUVECs do not express the receptors FCRI and FCRII, which have
been shown to bind to CRP. Furthermore, our results clearly show that
the effects of CRP are dependent on the presence of serum. Thus, it is
possible that CRP effects are dependent on 1 or more serum cofactors.
However, this mechanism does not appear to be species specific, because
similar results have been obtained with human and bovine serum (data
not shown). Further studies are needed to elucidate the basic
mechanisms of the proinflammatory effects of CRP on
endothelial cells.
In conclusion, CRP, at concentrations frequently observed in high-risk subjects and in patients with unstable angina, induces significant expression of adhesion molecules by human endothelial cells. These results suggest that CRP is not merely a marker of inflammation but has complex modulatory functions that may contribute to the development and evolution of inflammation/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 August 10, 2000; revision received September 8, 2000; accepted September 12, 2000.
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F. Anan, T. Masaki, Y. Umeno, T. Iwao, H. Yonemochi, N. Eshima, T. Saikawa, and H. Yoshimatsu Correlations of high-sensitivity C-reactive protein and atherosclerosis in Japanese type 2 diabetic patients Eur. J. Endocrinol., September 1, 2007; 157(3): 311 - 317. [Abstract] [Full Text] [PDF]
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I. Barutcu, A. T. Sezgin, N. Sezgin, H. Gullu, A. M. Esen, E. Topal, R. Ozdemir, F. Kosar, and S. Cehreli Increased High Sensitive CRP Level and Its Significance in Pathogenesis of Slow Coronary Flow Angiology, September 1, 2007; 58(4): 401 - 407. [Abstract] [PDF]
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H. Teoh, A. Quan, and S. Verma Does C-reactive protein predict saphenous vein graft patency? J. Thorac. Cardiovasc. Surg., August 1, 2007; 134(2): 277 - 279. [Full Text] [PDF]
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E. Grad, M. Golomb, I. Mor-Yosef, N. Koroukhov, C. Lotan, E. R. Edelman, and H. D. Danenberg Transgenic expression of human C-reactive protein suppresses endothelial nitric oxide synthase expression and bioactivity after vascular injury Am J Physiol Heart Circ Physiol, July 1, 2007; 293(1): H489 - H495. [Abstract] [Full Text] [PDF]
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J. D. Knudson, G. M. Dick, and J. D. Tune Adipokines and Coronary Vasomotor Dysfunction Experimental Biology and Medicine, June 1, 2007; 232(6): 727 - 736. [Abstract] [Full Text] [PDF]
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S. Ryan, G. M Nolan, E. Hannigan, S. Cunningham, C. Taylor, and W. T McNicholas Cardiovascular risk markers in obstructive sleep apnoea syndrome and correlation with obesity Thorax, June 1, 2007; 62(6): 509 - 514. [Abstract] [Full Text] [PDF]
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M. W. Lorenz, P. Karbstein, H. S. Markus, and M. Sitzer High-Sensitivity C-Reactive Protein Is Not Associated With Carotid Intima-Media Progression: The Carotid Atherosclerosis Progression Study Stroke, June 1, 2007; 38(6): 1774 - 1779. [Abstract] [Full Text] [PDF]
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H. Oren, A. R. Erbay, M. Balci, and S. Cehreli Role of Novel Biomarkers of Inflammation in Patients With Stable Coronary Heart Disease Angiology, April 1, 2007; 58(2): 148 - 155. [Abstract] [PDF]
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C. Rocker, D. E. Manolov, E. V. Kuzmenkina, K. Tron, H. Slatosch, J. Torzewski, and G. U. Nienhaus Affinity of C-Reactive Protein toward Fc{gamma}RI Is Strongly Enhanced by the {gamma}-Chain Am. J. Pathol., February 1, 2007; 170(2): 755 - 763. [Abstract] [Full Text] [PDF]
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F. Blaschke, Y. Takata, E. Caglayan, A. Collins, P. Tontonoz, W. A. Hsueh, and R. K. Tangirala A Nuclear Receptor Corepressor-Dependent Pathway Mediates Suppression of Cytokine-Induced C-Reactive Protein Gene Expression by Liver X Receptor Circ. Res., December 8, 2006; 99(12): e88 - e99. [Abstract] [Full Text] [PDF]
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M. Rahmani, R. P. Cruz, D. J. Granville, and B. M. McManus Allograft Vasculopathy Versus Atherosclerosis Circ. Res., October 13, 2006; 99(8): 801 - 815. [Abstract] [Full Text] [PDF]
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M. Suzuki, M. Saito, T. Nagai, H. Saeki, and Y. Kazatani Systemic Versus Coronary Levels of Inflammation in Acute Coronary Syndromes Angiology, August 1, 2006; 57(4): 459 - 463. [Abstract] [PDF]
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I. Kovacs, J. Toth, J. Tarjan, and A. Koller Correlation of flow mediated dilation with inflammatory markers in patients with impaired cardiac function. Beneficial effects of inhibition of ACE Eur J Heart Fail, August 1, 2006; 8(5): 451 - 459. [Abstract] [Full Text] [PDF]
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M. Juonala, J. S.A. Viikari, T. Ronnemaa, L. Taittonen, J. Marniemi, and O. T. Raitakari Childhood C-Reactive Protein in Predicting CRP and Carotid Intima-Media Thickness in Adulthood: The Cardiovascular Risk in Young Finns Study Arterioscler Thromb Vasc Biol, August 1, 2006; 26(8): 1883 - 1888. [Abstract] [Full Text] [PDF]
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L. M. Biasucci and V. Rizzello Pregnancy-associated plasma protein-a: do specific markers of vascular or plaque activation exist, and do we really need them? Clin. Chem., June 1, 2006; 52(6): 913 - 914. [Full Text] [PDF]
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J. Montaner, I. Fernandez-Cadenas, C. A. Molina, M. Ribo, R. Huertas, A. Rosell, A. Penalba, L. Ortega, P. Chacon, and J. Alvarez-Sabin Poststroke C-Reactive Protein Is a Powerful Prognostic Tool Among Candidates for Thrombolysis Stroke, May 1, 2006; 37(5): 1205 - 1210. [Abstract] [Full Text] [PDF]
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L. M. O'Brien, L. D. Serpero, R. Tauman, and D. Gozal Plasma adhesion molecules in children with sleep-disordered breathing. Chest, April 1, 2006; 129(4): 947 - 953. [Abstract] [Full Text] [PDF]
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