Monomeric C-Reactive Protein Generation on Activated Platelets: The Missing Link Between Inflammation and Atherothrombotic Risk

Trends in Cardiovascular Medicine

Volumn 19, Issue 7, 2009, Pages 232-237

  Eisenhardt, Steffen U ^a,b   Habersberger, Jonathon ^a   Peter, Karlheinz ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; CD16 ANTIGEN; INTERLEUKIN 1; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; ROSUVASTATIN;

ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CLINICAL TRIAL; CONFORMATIONAL TRANSITION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE MARKER; HUMAN; INFLAMMATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REVIEW; RISK ASSESSMENT; RISK FACTOR; THROMBOCYTE ACTIVATION; THROMBOSIS;

ATHEROSCLEROSIS; BLOOD PLATELETS; C-REACTIVE PROTEIN; COMPLEMENT ACTIVATION; INFLAMMATION; PLATELET ACTIVATION; PROTEIN CONFORMATION; PROTEIN ISOFORMS; RISK FACTORS; THROMBOSIS;

EID: 77951286180     PISSN: 10501738     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tcm.2010.02.002     Document Type: Review

References (70)

1. Ballantyne C.M., Hoogeveen R.C., Bang H., et al. Lipoprotein-associated phospholipase A2, high-sensitivity C-reactive protein, and risk for incident coronary heart disease in middle-aged men and women in the Atherosclerosis Risk in Communities (ARIC) study. Circulation 2004, 109:837-842.
2. Best L.G., Zhang Y., Lee E.T., et al. C-reactive protein as a predictor of cardiovascular risk in a population with a high prevalence of diabetes: the Strong Heart Study. Circulation 2005, 112:1289-1295.
3. Brown D.A., Breit S.N., Buring J., et al. Concentration in plasma of macrophage inhibitory cytokine-1 and risk of cardiovascular events in women: a nested case-control study. Lancet 2002, 359:2159-2163.
4. Curb J.D., Abbott R.D., Rodriguez B.L., et al. C-reactive protein and the future risk of thromboembolic stroke in healthy men. Circulation 2003, 107:2016-2020.
5. Devaraj S., Davis B., Simon S.I., et al. CRP promotes monocyte-endothelial cell adhesion via Fcgamma receptors in human aortic endothelial cells under static and shear flow conditions. Am J Physiol Heart Circ Physiol 2006, 291:H1170-H1176.
6. Eisenhardt S.U., Habersberger J., Murphy A., et al. Dissociation of pentameric to monomeric C-reactive protein on activated platelets localizes inflammation to atherosclerotic plaques. Circ Res 2009, 105:128-137.
7. Eisenhardt S.U., Schwarz M., Bassler N., et al. Subtractive single-chain antibody (scFv) phagedisplay: tailoring phage-display for high specificity against function-specific conformations of cell membrane molecules. Nature Protocols 2007, 2:3063-3073.
8. Eisenhardt S.U., Schwarz M., Schallner N., et al. Generation of activation-specific human anti-alphaM/beta2 single-chain antibodies as potential diagnostic tools and therapeutic agents. Blood 2007, 109:3521-3528.
9. Fujii H., Li S.H., Szmitko P.E., Fedak P.W., et al. C-reactive protein alters antioxidant defenses and promotes apoptosis in endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2006, 26:2476-2482.
10. Gabay C., Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 1999, 340:448-454.
11. Gawaz M., Langer H., May A.E. Platelets in inflammation and atherogenesis. J Clin Invest 2005, 115:3378-3384.
12. Gill R., Kemp J.A., Sabin C., et al. Human C-reactive protein increases cerebral infarct size after middle cerebral artery occlusion in adult rats. J Cereb Blood Flow Metab 2004, 24:1214-1218.
13. Griselli M., Herbert J., Hutchinson W.L., et al. C-reactive protein and complement are important mediators of tissue damage in acute myocardial infarction. J Exp Med 1999, 190:1733-1740.
14. Haimovich B., Ji P., Ginalis E., et al. Phospholipase A2 enzymes regulate alpha IIb beta3-mediated, but not Fc gammaRII receptor-mediated, pp125FAK phosphorylation in platelets. Thromb Haemost 1999, 81:618-624.
15. Hansson G.K., Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006, 6:508-519.
16. Heuertz R.M., Schneider G.P., Potempa L.A., et al. Native and modified C-reactive protein bind different receptors on human neutrophils. Int J Biochem Cell Biol 2005, 37:320-335.
17. Hirschfield G.M., Gallimore J.R., Kahan M.C., et al. Transgenic human C-reactive protein is not proatherogenic in apolipoprotein E-deficient mice. Proc Natl Acad Sci U S A 2005, 102:8309-8314.
18. Huo Y., Schober A., Forlow S.B., et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med 2003, 9:61-67.
19. Inoue T., Kato T., Uchida T., et al. Local release of C-reactive protein from vulnerable plaque or coronary arterial wall injured by stenting. J Am Coll Cardiol 2005, 46:239-245.
20. Ji S.R., Ma L., Bai C.J., et al. Monomeric C-reactive protein activates endothelial cells via interaction with lipid raft microdomains. FASEB J 2009, 23:1806-1816.
21. Ji S.R., Wu Y., Zhu L., et al. Cell membranes and liposomes dissociate C-reactive protein (CRP) to form a new, biologically active structural intermediate: mCRP(m). FASEB J 2007, 21:284-294.
22. Jialal I., Devaraj S., Singh U. Sources of CRP in atherosclerotic lesions. Am J Pathol 2006, 168:1054-1055. [author reply 1055-1056].
23. Jialal I., Devaraj S., Venugopal S.K. C-reactive protein: risk marker or mediator in atherothrombosis?. Hypertension 2004, 44:6-11.
24. Khreiss T., Jozsef L., Hossain S., et al. Loss of pentameric symmetry of C-reactive protein is associated with delayed apoptosis of human neutrophils. J Biol Chem 2002, 277:40775-40781.
25. Khreiss T., Jozsef L., Potempa L.A., et al. Conformational rearrangement in C-reactive protein is required for proinflammatory actions on human endothelial cells. Circulation 2004, 109:2016-2022.
26. Khreiss T., Jozsef L., Potempa L.A., et al. Opposing effects of C-reactive protein isoforms on shear-induced neutrophil-platelet adhesion and neutrophil aggregation in whole blood. Circulation 2004, 110:2713-2720.
27. Khreiss T., Jozsef L., Potempa L.A., et al. Loss of pentameric symmetry in C-reactive protein induces interleukin-8 secretion through peroxynitrite signaling in human neutrophils. Circ Res 2005, 97:690-697.
28. Kim S.J., Gershov D., Ma X., et al. I-PLA(2) activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J Exp Med 2002, 196:655-665.
29. Koenen R.R., Von Hundelshausen P., Nesmelova I.V., et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009, 15:97-103.
30. Koenig W., Lowel H., Baumert J., et al. C-reactive protein modulates risk prediction based on the Framingham Score: implications for future risk assessment: results from a large cohort study in southern Germany. Circulation 2004, 109:1349-1353.
31. Koenig W., Sund M., Frohlich M., et al. C-reactive protein, a sensitive marker of inflammation, predicts future risk of coronary heart disease in initially healthy middle-aged men: results from the MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) Augsburg Cohort Study, 1984 to 1992. Circulation 1999, 99:237-242.
32. Koike T., Kitajima S., Yu Y., et al. Human C-reactive protein does not promote atherosclerosis in transgenic rabbits. Circulation 2009, 120:2088-2094.
33. Kovacs A., Tornvall P., Nilsson R., et al. Human C-reactive protein slows atherosclerosis development in a mouse model with human-like hypercholesterolemia. Proc Natl Acad Sci U S A 2007, 104:13768-13773.
34. 2 and lysophosphatidylcholine in the coronary circulation: association with early coronary atherosclerosis and endothelial dysfunction in humans. Circulation 2007, 115:2715-2721.
35. Maier W., Altwegg L.A., Corti R., et al. Inflammatory markers at the site of ruptured plaque in acute myocardial infarction: locally increased interleukin-6 and serum amyloid A but decreased C-reactive protein. Circulation 2005, 111:1355-1361.
36. Massberg S., Brand K., Gruner S., et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med 2002, 196:887-896.
37. Meuwissen M., van der Wal A.C., Niessen H.W., et al. Colocalisation of intraplaque C reactive protein, complement, oxidised low density lipoprotein, and macrophages in stable and unstable angina and acute myocardial infarction. J Clin Pathol 2006, 59:196-201.
38. Mineo C., Gormley A.K., Yuhanna I.S., et al. FcgammaRIIB mediates C-reactive protein inhibition of endothelial NO synthase. Circ Res 2005, 97:1124-1131.
39. Molins B., Pena E., Vilahur G., et al. C-reactive protein isoforms differ in their effects on thrombus growth. Arterioscler Thromb Vasc Biol 2008, 28:2239-2246.
40. 2 and its association with cardiovascular outcomes in patients with acute coronary syndromes in the PROVE IT-TIMI 22 (PRavastatin Or atorVastatin Evaluation and Infection Therapy-Thrombolysis In Myocardial Infarction) trial. Circulation 2006, 113:1745-1752.
41. 2 activity is associated with risk of coronary heart disease and ischemic stroke: the Rotterdam Study. Circulation 2005, 111:570-575.
42. Ortiz M.A., Campana G.L., Woods J.R., et al. Continuously-infused human C-reactive protein is neither proatherosclerotic nor proinflammatory in apolipoprotein E-deficient mice. Exp Biol Med (Maywood) 2009, 234:624-631.
43. Pai J.K., Pischon T., Ma J., et al. Inflammatory markers and the risk of coronary heart disease in men and women. N Engl J Med 2004, 351:2599-2610.
44. Paul A., Ko K.W., Li L., et al. C-reactive protein accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice. Circulation 2004, 109:647-655.
45. Pepys M.B., Hirschfield G.M., Tennent G.A., et al. Targeting C-reactive protein for the treatment of cardiovascular disease. Nature 2006, 440:1217-1221.
46. Potempa L.A., Maldonado B.A., Laurent P., et al. Antigenic, electrophoretic and binding alterations of human C-reactive protein modified selectively in the absence of calcium. Mol Immunol 1983, 20:1165-1175.
47. Potempa L.A., Zeller J.M., Fiedel B.A., et al. Stimulation of human neutrophils, monocytes, and platelets by modified C-reactive protein (CRP) expressing a neoantigenic specificity. Inflammation 1988, 12:391-405.
48. Reifenberg K., Lehr H.A., Baskal D., et al. Role of C-reactive protein in atherogenesis: can the apolipoprotein E knockout mouse provide the answer?. Arterioscler Thromb Vasc Biol 2005, 25:1641-1646.
49. Ridker P.M., Buring J.E., Rifai N. Soluble P-selectin and the risk of future cardiovascular events. Circulation 2001, 103:491-495.
50. Ridker P.M., Buring J.E., Shih J., et al. Prospective study of C-reactive protein and the risk of future cardiovascular events among apparently healthy women. Circulation 1998, 98:731-733.
51. Ridker P.M., Cushman M., Stampfer M.J., et al. Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med 1997, 336:973-979.
52. Ridker P.M., Danielson E., Fonseca F.A., et al. Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein. N Engl J Med 2008, 359:2195-2207.
53. Ridker P.M., Danielson E., Fonseca F.A., et al. Reduction in C-reactive protein and LDL cholesterol and cardiovascular event rates after initiation of rosuvastatin: a prospective study of the JUPITER trial. Lancet 2009, 373:1175-1182.
54. Ridker P.M., Hennekens C.H., Buring J.E., et al. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med 2000, 342:836-843.
55. Ridker P.M., Rifai N., Pfeffer M., et al. Elevation of tumor necrosis factor-alpha and increased risk of recurrent coronary events after myocardial infarction. Circulation 2000, 101:2149-2153.
56. Ridker P.M., Rifai N., Rose L., et al. Comparison of C-reactive protein and low-density lipoprotein cholesterol levels in the prediction of first cardiovascular events. N Engl J Med 2002, 347:1557-1565.
57. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 1999, 340:115-126.
58. Schonbeck U., Varo N., Libby P., et al. Soluble CD40L and cardiovascular risk in women. Circulation 2001, 104:2266-2268.
59. Schwedler S.B., Amann K., Wernicke K., et al. Native C-reactive protein increases whereas modified C-reactive protein reduces atherosclerosis in apolipoprotein E-knockout mice. Circulation 2005, 112:1016-1023.
60. Shine B., De Beer F.C., Pepys M.B. Solid phase radioimmunoassays for human C-reactive protein. Clin Chim Acta 1981, 117:13-23.
61. Shrive A.K., Cheetham G.M., Holden D., et al. Three dimensional structure of human C-reactive protein. Nat Struct Biol 1996, 3:346-354.
62. Slevin M., Matou-Nasri S., Turu M., et al. Modified C-reactive protein is expressed by stroke neovessels and is a potent activator of angiogenesis in vitro. Brain Pathol 2009, [Epub ahead of print].
63. Sun H., Koike T., Ichikawa T., et al. C-reactive protein in atherosclerotic lesions: its origin and pathophysiological significance. Am J Pathol 2005, 167:1139-1148.
64. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet 2009, The Emerging Risk Factors Collaboration, [Epub ahead of print].
65. Von Hundelshausen P., Weber C. Platelets as immune cells: bridging inflammation and cardiovascular disease. Circ Res 2007, 100:27-40.
66. Whiteley W., Jackson C., Lewis S., et al. Inflammatory markers and poor outcome after stroke: a prospective cohort study and systematic review of interleukin-6. PLOS Med 2009, [Epub ahead of print].
67. Woollard K.J., Phillips D.C., Griffiths H.R. Direct modulatory effect of C-reactive protein on primary human monocyte adhesion to human endothelial cells. Clin Exp Immunol 2002, 130:256-262.
68. Xie L., Chang L., Guan Y., et al. C-reactive protein augments interleukin-8 secretion in human peripheral blood monocytes. J Cardiovasc Pharmacol 2005, 46:690-696.
69. Yasojima K., Schwab C., McGeer E.G., et al. Generation of C-reactive protein and complement components in atherosclerotic plaques. Am J Pathol 2001, 158:1039-1051.
70. Zouki C., Haas B., Chan J.S., et al. Loss of pentameric symmetry of C-reactive protein is associated with promotion of neutrophil-endothelial cell adhesion. J Immunol 2001, 167:5355-5361.