C-reactive protein and inflammation: Conformational changes affect function

Biological Chemistry

Volumn 396, Issue 11, 2015, Pages 1181-1197

  Wu, Yi ^b   Potempa, Lawrence A ^c   El Kebir, Driss ^a   Filep, János G ^a  

^a MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^b LANZHOU UNIVERSITY   (China)

^c ROOSEVELT UNIVERSITY   (United States)

Author keywords

CRP derived peptides; innate immunity; monomeric CRP; pentameric CRP; resolution of inflammation

Indexed keywords

C REACTIVE PROTEIN;

ACUTE PHASE RESPONSE; BINDING SITE; COMPLEMENT ACTIVATION; CONFORMATIONAL TRANSITION; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; GENETIC TRANSCRIPTION; HUMAN; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; ISOMER; MACROPHAGE; MONOCYTE; MUTATIONAL ANALYSIS; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; THROMBOCYTE; ANIMAL; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION;

ANIMALS; C-REACTIVE PROTEIN; HUMANS; INFLAMMATION; PROTEIN CONFORMATION;

EID: 84945183855     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2015-0149     Document Type: Review

References (151)

1. Abernathy, T.J., Avery, O.T. (1941). The occurrence during acute infections of a protein not normally present in the blood: I. Distribution of the reactive protein in patients' sera and the effect of calcium on the flocculation reaction with C-polysaccharide of pneumococcus. J. Exp. Med. 73, 173-182.
2. Agrawal, A., Shrive, A.K., Greenhough, T.J., Volanakis, J.E. (2001). Topology and structure of the C1q-binding site on C-reactive protein. J. Immunol. 166, 3998-4004.
3. Ahrens, I., Domeij, H., Eisenhardt, S.U., Topcic, D., Albrecht, M., Leitner, E., Viitaniemi, K., Jowett, J.B., Lappas, M., Bode, C., et al. (2011). Opposing effects of monomeric and pentameric C-reactive protein on endothelial progenitor cells. Basic Res. Cardiol. 106, 879-895.
4. Asztalos B.F., Horan, M.S., Horvath, K.V., Mcdermott, A.Y., Chalasani, N.P., Schaefer, E.J. (2014). Obesity associated molecular forms of C-reactive protein in human. PLoS One 9, e109238.
5. Bang, R., Marnell, L., Mold, C., Stein, M.-P., Du Clos, K.T., Chivington-Buck, C., Du Clos, T.W. (2005). Analysis of binding sites in human C-reactive protein for FcRI, FcRIIA, and C1q by site-directed mutagenesis. J. Biol. Chem. 280, 25095-25102.
6. Bharadwaj, D., Stein, M.-P., Volzer, M.A., Burlingame, R.W., Du Clos, T.W. (1999). The major receptor for C-reactive protein on leukocytes is Fcreceptor II. J. Exp. Med. 190, 585-590.
7. Bisoendial, R.J., Kastelein, J.J., Levels, J.H., Zwaginga, J.J., van den Bogaard, B., Reitsma, P.H., Meijers, J.C., Hartman, D., Levi, M., Stroes, E.S. (2005). Activation of inflammation and coagulation after infusion of C-reactive protein in humans. Circ. Res. 96, 714-716.
8. Bisoendial, R.J., Kastelein, J.J., Peters, S.L., Levels, J.H., Birjmohun, R., Rotmans, J.I., Hartman, D., Meijers, J.C., Levi, M., Stroes, E.S. (2007). Effects of CRP infusion on endothelial function and coagulation in normocholesterolemic and hypercholesterolemic subjects. J. Lipid Res. 48, 952-960.
9. Black, S., Kushner, I., Samols, D. (2004). C-reactive protein. J. Biol. Chem. 279, 48487-48490.
10. Brennan, M.P., Moriarty, R.D., Grennan, S., Chubb, A.J., Cox, D. (2008) C-reactive protein binds to IIb3. J. Thromb. Haemost. 6, 1239-1241.
11. Calabro, P., Willerson, J.T., Yeh, E.T. (2003). Inflammatory cytokines stimulated C-reactive protein production by human coronary artery smooth muscle cells. Circulation 108, 1930-1932.
12. Casas, J.P., Shah, T., Hingorani, A.D., Danesh, J., Pepys, M.B. (2008). C-reactive protein and coronary heart disease: a critical review. J. Intern. Med. 264, 295-314.
13. Chang, M.K., Binder, C.J., Torzewski, M., Witztum, J. (2002). C-reactive protein binds to both oxidized LDL and apoptotic cells through recognition of a common ligand: phosphorylcholine of oxidized phospholipids. Proc. Natl. Acad. Sci. USA 99, 13043-13048.
14. Chen, J., Huang, L., Song, M., Yu, S., Gao, P., Jing, J. (2009). C-reactive protein upregulates receptor for advanced glycation end products expression and alters antioxidant defenses in rat endothelial progenitor cells. J. Cardiovasc. Pharmacol. 53, 359-367.
15. Ciubotaru, I., Potempa, L.A., Wander, R.C. (2005). Production of modified C-reactive protein in U937-derived macrophages. Exp. Biol. Med. (Maywood) 230, 762-770.
16. Crawford, D.C., Sanders, C.L., Qin, X., Smith, J.D., Shephard, C., Wong, M., Witrak, L., Rieder, M.J., Nickerson, D.A. (2006). Genetic variation is associated with C-reactive protein levels in the third national health and nutrition examination survey. Circulation 114, 2458-2465.
17. C-Reactive Protein Coronary Heart Disease Genetics Collaboration (CCGC), Wensley F., Gao P., Burgess S., Kaptoge S., Di Angelantonio E., Shah T., Engert J.C., Clarke R., Davey-Smith G., et al. (2011) Association between C reactive protein and coronary heart disease: mendelian randomisation analysis based on individual participant data. Br. Med. J. 342, d548.
18. Devaraj, S., Jialal, I. (2011). C-reactive protein polarizes human macrophages to an M1 phenotype and inhibits transformation to the M2 phenotype. Arterioscler. Thromb. Vasc. Biol. 31, 1397-1402.
19. Devaraj, S., Xu, D.Y., Jialal, I. (2003). C-reactive protein increases plasminogen activator inhibitor-1 expression and activity in human aortic endothelial cells: Implications for the metabolic syndrome and atherothrombosis. Circulation 107, 398-404.
20. Devaraj, S., Du Clos, T.W., Jialal, I. (2005). Binding and internalization of C-reactive protein by Fc gamma receptors on human aortic endothelial cells mediates biological effects. Arterioscler. Thromb. Vasc. Biol. 25, 1359-1363.
21. Devaraj, S., Davis, B., Simon, S.I., Jialal, I. (2006). CRP promotes monocyte-endothelial cell adhesion via Fc receptors in human aortic endothelial cells under static and shear flow conditions. Am. J. Physiol. Heart Circ. Physiol. 291, H1170-H1176.
22. Diehl, E.E., Haines, G.K. III, Radosevich, J.A., Potempa, L.A. (2000). Immunohistochemical localization of modified C-reactive protein antigen in normal vascular tissue. Am. J. Med. Sci. 319, 79-83.
23. El Kebir, D., Zhang, Y., Potempa, L.A., Wu, Y., Fournier, A., Filep, J.G. (2011). C-reactive protein-derived peptide 201-206 inhibits neutrophil adhesion to endothelial cells and platelets through CD32. J. Leukoc. Biol. 90, 1167-1175.
24. Eisenhardt, S.U., Habersberger, J., Murphy, A., Chen, Y.C., Woollard, K.J., Bassler, N., Qian, H., von zur Muhlen, C., Hagemeyer, C.E., Ahrens, I., et al. (2009). Dissociation of pentameric to monomeric C-reactive protein on activated platelets localizes inflammation to atherosclerotic plaques. Circ. Res. 105, 128-137.
25. Fadi, G., Oparil, S., Xing, D., Chen, Y.-F., McCrory, M.A., Szalai, A.J. (2010). C-reactive protein-mediated vascular injury requires complement. Arterioscler. Thromb. Vasc. Biol. 30, 1189-1195.
26. Filep, J.G. (2009). Platelets affect the structure and function of C-reactive protein. Circ. Res. 105, 109-111.
27. Filep, J.G., El Kebir, D. (2009). Neutrophil apoptosis: a target for enhancing the resolution of inflammation. J. Cell. Biochem. 108, 1039-1046.
28. Fu, T., Borensztajn, J. (2002). Macrophage uptake of low-density lipoprotein bound to aggregated C-reactive protein: possible mechanism of foam-cell formation in atherosclerotic lesions. Biochem. J. 366, 195-201.
29. Fujii, H., Li, S.H., Szmitko, P.E., Fedak, P.W., Verma, S. (2006). C-reactive protein alters antioxidant defenses and promotes apoptosis in endothelial progenitor cells. Arterioscler. Thromb. Vasc. Biol. 26, 2476-2482.
30. Fujita, Y., Kakino, A., Nishimichi, N., Yamaguchi, S., Sato, Y., Machida, S., Cominacini, L., Delneste, Y., Matsuda, H., Sawamura, T. (2009). Oxidized LDL receptor LOX-1 binds to C-reactive protein and mediates its vascular effects. Clin. Chem. 55, 285-294.
31. Fujita, M., Takada, Y.K., Izumiya, Y., Takada, Y. (2014). The binding of monomeric C-reactive protein (mCRP) to integrins V3 and 41 is related to its pro-inflammatory action. PLoS One 9, e93738.
32. Gabay, C., Kushner, I. (1999). Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 340, 448-454.
33. Gershov, D., Kim, S.J., Brot, N., Elkon, K.B. (2000) C-reactive protein binds to apoptotic cells, protects the cells from the assembly of the terminal complement components, and sustains an antiinflamamtory innate immune response. J. Exp. Med. 192, 1353-1364.
34. Gill, R., Kemp, J.A., Sabin, C., Pepys, M.B. (2004). Human C-reactive protein increases cerebral infarct size after middle cerebral artery occlusion in adult rats. J. Cereb. Blood Flow Metab. 24, 1214-1218.
35. Griselli, H., Herbert, J., Hutchinson, W.L., Taylor, K.M., Sohail, M., Krausz, T., Pepys, M.B. (1999). C-reactive protein and complement are important mediators of tissue damage in acute myocardial infarction. J. Exp. Med. 190, 1733-1740.
36. Habersberger, J., Strang, F., Scheichl, A., Htun, N., Bassler, N., Merivirta, R.-M., Diehl, P., Krippner, G., Meikle, P., Eisenhardt, S.U., et al. (2012). Circulating microparticles generate and transport monomeric C-reactive protein in patients with myocardial infarction. Cardiovasc. Res. 96, 64-72.
37. Hage, F.G., Oparil, S., Xing, D., Chen, Y.-F., McCrory, M.A., Szalai, A.J. (2010). C-reactive protein-mediated vascular injury requires complement. Arterioscler. Thromb. Vasc. Biol. 30, 1189-1195.
38. Hammond, D.J. Jr., Singh, S.K., Thompson, J.A., Beeler, B.W., Rusinol, A.E., Pangburn, M.K., Potempa, L.A., Agrawal, A. (2010). Identification of acidic pH-dependent ligands of pentameric C-reactive protein. J. Biol. Chem. 285, 36235-36244.
39. Han, K.H., Hong, K.H., Park, J.H., Ko, J., Kang, D.H., Choi, K.J., Hong, M.K., Park, S.W., Park, S.J. (2004). C-reactive protein promotes monocyte chemoattractant protein-1-mediated chemotaxis through up-regulating CC chemokine receptor 2 expression in human monocytes. Circulation 109, 2566-2571.
40. Hanriot, D., Bello, G., Ropars, A., Seguin-Devaux, C., Poitevin, G., Grosjean, S., Latger-Cannard, V., Devaux, Y., Zanmad, F., Regnault, V., et al. (2008). C-reactive protein induces pro-and anti-inflammatory effects, including activation of the liver X receptor , on human monocytes. Thromb. Haemost. 99, 558-569.
41. Hanson, K.G., Libby, P. (2006). The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 6, 508-519.
42. Heuertz, R.M., Ahmed, N., Webster, R.O. (1996). Peptides derived from C-reactive protein inhibit neutrophil alveolitis. J. Immunol. 156, 3412-3417.
43. Heuertz, R.M., Schneider, G.P., Potempa, L.A., Webster, R.O. (2005). Native and modified C-reactive proteins bind different receptors on human neutrophils. Int. J. Biochem. Cell Biol. 37, 320-335.
44. Hill, J.M., Zalos, G., Halcox, J.P., Schenke, W.H., Waclawiw, M.A., Quyyumi, A.A., Finkel, T. (2003). Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N. Engl. J. Med. 348, 593-600.
45. Hirschfield, G.M., Gallimore, J.R., Kahan, M.C., Hutchinson, W.L., Sabin, C.A., Benson, G.M., Dhillon, A.P., Tennent, G.A., Pepys, M.B. (2005). Transgenic human C-reactive protein is not proatherogenic in apoplipoprotein E-deficient mice. Proc. Natl. Acad. Sci. USA 102, 8309-8014.
46. Jabs, W.J., Lering, B.A., Gerke, P., Kreft, B., Wolber, E.M., Klinger, M.H., Fricke, L., Steinhoff, J. (2003a). The kidney as a second site of human C-reactive protein formation in vivo. Eur. J. Immunol. 33, 152-161.
47. Jabs, W.J., Theissing, E., Nitschke, M., Bechtel, J.F., Duchrow, M., Mohamed, S., Jahrbeck, B., Sievers, H.H., Steinhoff, J., Bartels, C. (2003b). Local generation of C-reactive protein in diseased coronary artery venous bypass grafts and normal tissue. Circulation 108, 1428-1431.
48. Ji, S.-R., Wu, Y., Potempa, L.A., Liang, Y.-H., Zhao, J. (2006a) Effect of modified C-reactive protein on complement activation. Arterioscler. Thromb. Vasc. Biol. 26, 935-941.
49. Ji, S.R. Wu, Y., Potempa, L.A., Qiu, Q., Zhao, J. (2006b). The interactions of low density lipoprotein with different forms of C-reactive protein: implication of an active role of modified C-reactive protein in the pathogenesis of atherosclerosis. Int. J. Biochem. Cell Biol. 38, 648-661.
50. Ji, S.-R., Wu, Y., Zhu, L., Potempa, L.A., Sheng, F.L., Lu, W., Zhao, J. (2007). Cell membranes and liposomes dissociate C-reactive protein (CRP) to form a new, biologically active structural intermediate mCRP(m). FASEB J. 21, 284-294.
51. Ji, S.-R., Ma, L., Bai, C.J., Shi, J.M., Li, H.Y., Potempa, L.A., Filep, J.G., Zhao, J., Wu, Y. (2009). Monomeric C-reactive protein activates endothelial cells via interaction with lipid raft microdomains. FASEB J. 23, 1806-1816.
52. Kakuta, Y., Aoshiba, K., Nagai, A. (2006). C-reactive protein products generated by neutrophil elastase promote neutrophils apoptosis. Arch Med. Res. 37, 456-460.
53. Kaplan, M.J. (2009). Premature vascular damage in systemic lupus erythematosus. Autoimmunity 42, 580-586.
54. Kapur, R., Heitink-Poll K.M.J., Porcelijn, L., Bentlage, A.E.H., Bruin, M.C.A., Visser, R., Roos, D., Schasfoort, R.B.M., de Haas, M., van der Schoot, E., et al. (2015). C-reactive protein enhances IgG-mediated phagocyte responses and thrombocytopenia. Blood 125, 1793-1802.
55. Kardys, I., de Maat, M.P., Uitterlinden, A.G., Hofman, A., Witteman, J.C. (2006). C-reactive protein gene haplotypes and risk of coronary heart disease: the Rotterdam study. Eur. Heart J. 27, 1331-1337.
56. Khreiss, T., Jsef, L., Hossain, S., Chan, J.S.D., Potempa, L.A., Filep, J.G. (2002). Loss of pentameric symmetry of C-reactive protein is associated with delayed apoptosis of human neutrophils. J. Biol. Chem. 277, 40775-40781.
57. Khreiss, T., Jsef, L., Potempa, L.A., Filep, J.G. (2004a). Conformational rearrangement in C-reactive protein is required for proinflammatory actions on human endothelial cells. Circulation 109, 2016-2022.
58. Khreiss, T., Jsef, L., Potempa, L.A., Filep, J.G. (2004b). Opposing effects of C-reactive protein isoforms on shearinduced neutrophil-platelet adhesion and neutrophil aggregation in whole blood. Circulation 110, 2713-2720.
59. Khreiss, T., Jsef, L., Potempa, L.A., Filep, J.G. (2005). Loss of pentameric symmetry in C-reactive protein induces interleukin-8 secretion through peroxynitrite signalling in human neutrophils. Circ. Res. 97, 690-697.
60. Koenig, W. (2013). High-sensitivity C-reactive protein and atherosclerotic disease: from improved risk prediction to risk-guided therapy. Int. J. Cardiol. 168, 5126-5134.
61. Kovacs, A., Tornwall, P., Nilsson, R., Tegner, J., Hamsten, A., Bjorkegren, J. (2007). Human C-reactive protein slows atherosclerosis development in a mouse model with humanlike hypercholesterolemia. Proc. Natl. Acad. Sci. USA 104, 13768-13773.
62. Kresl, J.J., Potempa, L.A., Anderson, B.E. (1998). Conversion of native oligomeric to a modified monomeric form of human C-reactive protein. Int. J. Biochem. Cell Biol. 30, 1415-1426.
63. Krijnen, P.A., Ciurana, C., Cramer, T., Hazes, T., Meijer, C.J., Visser, C.A., Niessen, H.W., Hack, C.E. (2005). IgM colocalizes with complement and C-reactive protein in infarcted myocardium. J. Clin. Pathol. 58, 382-388.
64. Lane, T., Wassef, N., Poole, S., Mistry, Y., Lachmann, H.J., Gillmore, J.D., Hawkins, P.N., Pepys, M.B. (2014). Infusion of pharmaceutical-grade natural human C-reactive protein is not proinflammatory in healthy adult human volunteers. Circ. Res. 114, 672-676.
65. Ley, K., Laudanna, C., Cybulsky, M.I., Noursargh, S. (2007). Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7, 678-689.
66. Li, L., Roumeliotis, N., Sawamura, T., Renier, G. (2004a). C-reactive protein enhances LOX-1 expression in human aortic endothelial cells: relevance of LOX-1 to C-reactive proteininduced endothelial dysfunction. Circ. Res. 95, 877-883.
67. Li, S.H., Szmitko, P.E., Weisel, R.D., Wang, C.H., Fedak, P.W., Li, R.K., Mickle, D.A., Verma, S. (2004b). C-reactive protein upregulates complement-inhibitory factors in endothelial cells. Circulation 109, 833-836.
68. Li, R., Ren, M., Luo, M., Chen, N., Zhang, Z., Luo, B., Wu, J. (2012). Monomeric C-reactive protein alters fibrin clot properties on endothelial cells. Thromb. Res. 129, e251-e256.
69. Li, H.-Y., Wang, J., Wu, Y.-X., Zhang, L., Liu, Z.-P., Filep, J.G., Potempa, L.A., Wu, Y., Ji, S.-R. (2014). Topological localization of monomeric C-reactive protein determines pro-inflammatory endothelial cell responses. J. Biol. Chem. 289, 14283-14290.
70. Lu, J., Marnell, L.L., Marjon, K.D., Mold, C., Du Clos, T.W., Sun, P.D. (2008). Structural recognition and functional activation of FcR by innate pentraxins. Nature 456, 989-993.
71. Lu, J., Marjon, K.D., Marnell, L.L., Wang, R., Mold, C., Du Clos, T.W., Sun P (2011). Recognition and functional activation of the human IgA receptor (FcalphaRI) by C-reactive protein. Proc. Natl. Acad. Sci. USA 108, 4974-4979.
72. Marnell, L.L., Mold, C., Volzer, M.A., Burlingame, R.W., Du Clos, T.W. (1995). C-reactive protein binds to FcRI in transfected COS cells. J. Immunol. 155, 2185-2193.
73. Marnell, L.L., Mold, C., Du Clos, T.W. (2005). C-reactive protein: ligands, receptors and role in inflammation. Clin. Immunol. 117, 104-111.
74. Mihlan, M., Blom, A.M., Kupreishvili, K., Lauer, N., Stelzner, K., Bergstr, F., Niessen, H.W.M., Zipfel, P.F. (2011). Monomeric C-reactive protein modulates classic complement activation on necrotic cells. FASEB J. 25, 4198-4210.
75. Mold, C., Rodic-Polic, B., Du Clos, T.W. (2002). Protection from Streptococcus pneumoniae infection by C-reactive protein and natural antibody requires complement but not Fcgamma receptors. J. Immunol. 168, 6375-6381.
76. Molins, B., Pe, E., Vilahur, G., Mandieta, C., Slevin, M., Badimon, L. (2008). C-reactive protein isoforms differ in their effects on thrombus growth. Arterioscler. Thromb. Vasc. Biol. 28, 2239-2246.
77. Molins, B., Pe, E., de la Torre, R., Badimon, L. (2011) Monomeric C-reactive protein is prothrombotic and dissociates from circulating pentameric C-reactive protein on adhered activated platelets under flow. Cardiovasc. Res. 92, 328-337.
78. Montecucco, F., Steffens, S., Burger, F., Pelli, G., Monaco, C., Mach, F. (2008). C-reactive protein (CRP) induces chemokine secretion via CD11b/ICAM-1 interaction in human adherent monocytes. J. Leukoc. Biol. 84, 1109-1119.
79. Monteiro, R.C., van den Winkel, J.G. (2003). IgA Fc receptors. Annu. Rev. Immunol. 21, 177-204.
80. Murray, P.J., Wynn, T.A. (2011). Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723-737.
81. Nathan, C., Ding, A. (2010). Nonresolving inflammation. Cell 140, 871-882.
82. Nimmerjahn, F., Ravetch, J.V. (2008). Fcreceptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47.
83. Noveck, R., Stroes, E.S.G., Flaim, J.D., Baker, B.F., Hughes, S., Graham, M.J., Crooke, R.M., Ridker, P.M. (2014). Effects of an antisense oligonucleotide inhibitor of C-reactive protein synthesis on the endotoxin challenge response in healthy human male volunteers. J. Am. Heart Assoc. 3, pii: e001084. doi:10.1161/JAHA.114.001084.
84. Okemefuna, A.I., Stach, L., Rana, S., Buetas, A.J., Gor, J., Perkins, S.J. (2010). C-reactive protein exists in an NaCl concentration-dependent pentamer-decamer equilibrium in physiological buffer. J. Biol. Chem. 285, 1041-1052.
85. Pasceri, V., Willerson, J.T., Yeh, E.T. (2000). Direct proinflammatory effect of C-reactive protein on human endothelial cells. Circulation 102, 2165-2168.
86. Pasceri, V., Cheng, J.S., Willerson, J.T., Yeh, ET. (2001). Modulation of C-reactive protein-mediated monocyte chemoattractant protein-1 induction in human endothelial cells by anti-atherosclerosis drugs. Circulation 103, 2531-2534.
87. Paul, A., Ko, K.W., Li, L., Yechoor, V., McCrory, M.A., Szalai, A.J., Chan, L. (2004). C-reactive protein accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice. Circulation 109, 647-655.
88. Pepys, M.B., Hirschfield, G.M. (2003) C-reactive protein: a critical update. J. Clin. Invest. 111, 805-1812.
89. Pepys, M.B., Hirschfield, G.M., Tennent, G.A., Gallimore, J.R., Kahan, M.C., Bellotti, V., Hawkins, P.N., Myers, R.M., Smith, M.D., Polara, A., et al. (2006). Targeting C-reactive protein for the treatment of cardiovascular disease. Nature 440, 1217-1221.
90. Perkins, S.J., Okemefuna, A.I., Nan, R. (2010) Unravelling protein-protein interactions between complement factor H and C-reactive protein using a multidisciplinary strategy. Biochem. Soc. Trans. 38, 894-900.
91. Pober, J.S., Sessa, W.C. (2007). Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 7, 803-815.
92. Potempa, L.A., Maldonado, B.A., Laurent, P., Zemel, E.S., Gewurz, H. (1983). Antigenic, electrophoretic and binding alterations of human C-reactive protein modified selectively in the absence of calcium. Mol. Immunol. 20, 1165-1175.
93. Qamirani, E., Ren, Y., Kuo, L., Hein, T.W. (2005). C-reactive protein inhibits endothelium-dependent NO-mediated dilation in coronary arterioles by activating p38 kinase and NAD(P)H oxidase. Arterioscler. Thromb. Vasc. Biol. 25, 995-1001.
94. Reynolds, G.D., Vance, R.P. (1987) C-reactive protein immunohistochemical localization in normal and atherosclerotic human aortas. Arch. Pathol. Lab. Med. 111, 265-269.
95. Rodriguez, W., Mold, C., Kataranovski, M., Hutt, J.A., Marnell, L.L., Verbeek, J.S., Du Clos T.W. (2007). C-reactive proteinmediated suppression of nephrotoxic nephritis: role of macrophages, complement, and Fcreceptors. J. Immunol. 178, 530-538.
96. Russell, A.I., Cunninghame Graham, D.S., Shepherd, C., Roberton, C.A., Whittaker, J., Meeks, J., Powell, R.J., Isenberg, D.A., Walport, M.J., Vyse, T.J. (2004). Polymorphism in the C-reactive protein locus influences gene expression and predisposes to systemic lupus erythematosus. Hum. Mol. Genet. 13, 137-147.
97. Schwartz, R., Osborne-Lawrence, S., Hahner, L., Gibson, L.H., Gormley, A.K., Vongpatanasin, W., Zhu, W., Word, A., Seetharam, D., Black, S., et al. (2007). C-reactive protein downregulates endothelial NO synthase and attenuates reendothelialization in vivo in mice. Circ. Res. 100, 1452-1459.
98. Schwedler, S.B., Guderian, F., Dammrich, J., Potempa, L.A., Wanner, C. (2003). Tubular staining of modified C-reactive protein in diabetic chronic kidney disease. Nephrol. Dial. Transplant. 18, 2300-2307.
99. Schwedler, S.B., Amann, K., Wernicke, K., Krebs, A., Nauck, M., Wanner, C., Potempa, L.A., Galle, J. (2005). Native C-reactive protein increases whereas modified C-reactive protein reduces atherosclerosis in apolipoprotein E-knockout mice. Circulation 112, 1016-1023.
100. Schwedler, S.B., Filep, J.G., Galle, J., Wanner, C., Potempa, L.A. (2006). C-reactive protein: a family of proteins to regulate cardiovascular function. Am. J. Kidney Dis. 47, 212-222.
101. Schwedler, S.B., Kuhlencordt, P.J., Ponnuswamy, P.P., Hatiboglu, G., Quaschning, T., Widder, J., Wanner, C., Potempa, L.A., Galle, J. (2007). Native C-reactive protein induces endothelial dysfunction in ApoE-/-mice: implications of iNOS and reactive oxygen species. Atherosclerosis 195, e76-e84.
102. Schwedler, S.B., Hansen-Hagge, T., Reichert, M., Schmiedeke, D., Schneider, R., Galle, J., Potempa, L.A., Wanner, C., Filep, J.G. (2009). Monomeric C-reactive protein decreases acetylated LDL uptake in human endothelial cells. Clin. Chem. 55, 1728-1731.
103. Scirica, B.M., Morrow, D.A. (2006). Is C-reactive protein an innocent bystander of proatherogenic culprit Circulation 113, 2128-2134.
104. Scott, J. (2007). The liver X receptor and atherosclerosis. N. Engl. J. Med. 357, 2195-2197.
105. Shephard, E.G., erson, R., Rosen, O., Myer, M.S., Friedkin, M., Strachan, A.F., de Beer, F.C. (1990). Peptides generated from C-reactive protein by a neutrophil membrane protease. Amino acid sequence and effects of peptides on neutrophil oxidative metabolism and chemotaxis. J. Immunol. 145, 1469-1476.
106. Shrive, A.K., Cheetham, M., Holden, D., Myles, D.A., Turnell, W.G., Volanakis, J.E., Pepys, M.B., Bloomer, A.C., Greenhough, T.J. (1996). Three dimensional structure of human C-reactive protein. Nat. Struct. Biol. 3, 346-354.
107. Sica, A., Mantovani, A. (2012). Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 122, 787-795.
108. Singh, U., Devaraj, S., Dasu, M.R., Ciobanu, D., Reusch, J., Jialal, I. (2006) C-reactive protein decreases interleukin-10 secretion in activated human monocyte-derived macrophages via inhibition of cyclic AMP production. Arterioscler. Trhomb. Vasc. Biol. 26, 2469-2475.
109. Singh, S.K., Suresh, M.V., Prayhter, D.C., Moorman, J.P., Rusinol, A.E., Agrawal, A. (2008). C-reactive proteinbound enzymatically modified low-density lipoprotein does not transform macrophages into foam cells. J. Immunol. 180, 4316-4322
110. Sjerg, A.P., Trouw, L.A., McGrath, F.D., Hack, C.E., Blom, A.M. (2006). Regulation of complement activation by C-reactive protein: targeting of the inhibitory activity of C4b-binding protein. J. Immunol. 176, 7612-7620
111. Sjall, C., Bengtsson, A.A., Sturfelt, G., Skogh, T. (2004). Serum levels of autoantibodies against monomeric C-reactive protein are correlated with disease activity in systemic lupus erythematosus. Arthritis res. Ther. 6, R87-R94.
112. Slevin, M., Matou-Nasri, S., Turu, M., Luque, A., Rovira, N., Badimon, L., Boluda, S., Potempa, L.A., Sanfeliu, C., de Vera, N., et al. (2010). Modified C-reactive protein is expressed by stroke neovessels and is a potent activator of angiogenesis in vitro. Brain Pathol. 20, 151-165.
113. Sreeramkumar, V., Adrover, J.M., Ballesteros, I., Cuartero, M.I., Rossaint, J., Bilbao, I., Nher, M., Pitaval, C., Radovanovic, I., Fukui, Y., et al. (2014). Neutrophils scan for activated platelet to initiate inflammation. Science 346, 1234-1238.
114. Stein, M.P., Edberg, J.C., Kimberly, R.P., Mangan, E.K., Bharadwaj, D., Mold, C., Du Clos, T.W. (2000). C-reactive protein binding to FcRIIa on human monocyte sand neutrophils is allele-specific. J. Clin. Invest. 105, 369-376.
115. Sternik, L., Samee, S., Schaff, H.V., Zehr, K.J., Lerman, L.O., Holmes, D.R., Hermann, J., Lerman, A. (2002). C-reactive protein relaxes human vessels in vitro. Arterioscler. Thromb. Vasc. Biol. 22, 1865-1868.
116. Strang, F., Scheichl, A., Chen, Y.C., Wang, X., Htun, N.M., Bassler, N., Eisenhardt, S.U., Habersberger, J., Peter, K. (2012). Amyloid plaques dissociate pentameric to monomeric C-reactive protein: a novel pathomechanism driving cortical inflammation in Alzheimer's disease Brain Pathol. 22, 337-346.
117. Sun, H., Koike, T., Ichikawa, T., Hatakeyama, K., Shiomi, M., Zhang, B., Kitajima, S., Morimoto, M., Watanabe, T., Asada, Y., et al. (2005). C-reactive protein in atherosclerotic lesions: its origin and pathophysiological significance. Am. J. Pathol. 167, 1139-1148.
118. Szalai, A.J., Nataf, S., Hu, X.Z., Barnum, S.R. (2002). Experimental allergic encephalomyelitis is inhibited in transgenic mice expressing human C-reactive protein. J. Immunol. 168, 5792-5797.
119. Szalai, A.J., Weaver, C.T., McCrory, M.A., van Ginkel, F.W., Reiman, R.M., Kearney, J.F., Marion, T.N., Volanakis, J.E. (2003). Delayed lupus onset in (NZBxNZF)F1 mice expressing a human C-reactive protein transgene. Arthritis Rheum. 48, 1602-1611.
120. Szalai, A.J., McCrory, M.A., Xing, D., Hage, F.G., Miller, A., Oparil, S., Chen, Y.-F., Mazzone, M., Early, R., Henry, S.P., et al. (2014). Inhibiting C-reactive protein for the treatment of cardiovascular disease: promising evidence from rodent models. Med. Inflamm. 2014, 353614.
121. Tanigaki, K., Mineo, C., Yuhanna, I.S., Chambliss, K.L., Quon, M.J., Bonvini, E., Shaul, P.W. (2007). C-reactive protein inhibits insulin activation of endothelial nitric oxide synthase via the immunoreceptor tyrosine-based inhibition motif of FcRIIB and SHIP-1. Circ. Res. 104, 1275-1282.
122. Teupser, D., Weber, O., Rao, T.N., Sass, K., Thiery, J., Fehling, H.J. (2011). No reduction of atherosclerosis in C-reactive protein (CRP)-deficient mice. J. Biol. Chem. 286, 6272-6279.
123. Thiele, J.R., Habersberger, J., Braig, D., Schmidt, Y., Goerendt, K., Maurer, V., Bannasch, H., Scheichl, A., Woolard, K., von Dobschz, E., et al. (2014). The dissociation of pentameric to monomeric C-reactive protein localizes and aggravates inflammation: in vivo proof of a powerful pro-inflammatory mechanisms and a new anti-inflammatory strategy. Circulation 130, 35-50.
124. Tilg, H., Vannier, E., Vachino, G., Dinarello, C.A., Mier, J.W. (1993). Antiinflammatory properties of hepatic acute phase proteins: preferential induction of interleukin 1 (IL-1) receptor antagonist over IL-1synthesis by human peripheral blood mononuclear cells. J. Exp. Med. 178, 1629-1636.
125. Tillett, W.S., Francis, T. (1930). Serological reactions in pneumonia with a non-protein somatic fraction of pneumococcus. J. Exp. Med. 52, 561-571.
126. Torzewski, J., Torzewski, M., Bowyer, D.E., Frich, M., Koenig, W., Waltenberger, J., Fitzsimmons, C., Hornbach, V. (1998). C-reactive protein frequently colocalizes with the terminal complement complex in the intima of early atherosclerotic lesions of human coronary arteries. Arterioscler. Thromb. Vasc. Biol. 18, 1386-1392.
127. Torzewski, M., Rist, C., Mortensen, R.F., Zwaka, T.P., Bienek, M., Waltenberger, J., Koenig, W., Schmitz, G., Hombach, V., Torzewski, J. (2000) C-reactive protein in the arterial intima: role of C-reactive protein receptor-dependent monocyte recruitment in atherogenesis. Arterioscler. Thromb. Vasc. Biol. 20, 2094-2099.
128. Trion, A., de Maat, M.P., Jukema, J.W., van der Laarse, A., Maas, M.C., Offerman, E.H., Havekes, L.M., Szalai. A.J., Princen, H.M., Emeis, J.J. (2005). No effect of C-reactive protein on early atherosclerosis development in apolipoprotein E 3-leiden/human C-reactive protein transgenic mice. Arterioscler. Thromb. Vasc. Biol. 25, 1635-1640.
129. Tsimikas, S., Willerson, J.T., Ridker, P.M. (2006). C-reactive protein and other emerging blood biomarkers to optimize risk stratification of vulnerable patients. J. Am. Coll. Cardiol. 47, C19-C31
130. van den Berg, C.W., Taylor, K.E., Lang, D. (2004). C-reactive protein-induced in vivo vasorelaxation is an artefect caused by the presence of sodium azide in commercial preparations. Arterioscler. Thromb. Vasc. Biol. 24, 158-171.
131. Venugopal, S.K., Devaraj, S., Yuhanna, I., Shaul, P., Jialal, I. (2002). Demonstration that C-reactive protein decreases eNOS expression and bioactivity in human aortic endothelial cells. Circulation 106, 1439-1441.
132. Verma, S., Kuliszewski, M.A., Li, S.H., Szmitko, P.E., Zucco, L., Wang, C.H., Badiwala, M.V., Mickle, D.A., Weisel, R.D., Fedak, P.W., et al. (2004). C-reactive protein attenuates endothelial progenitor cell survival, differentiation, and functionL further evidence of a mechanistic link between C-reactive protein and cardiovascular disease. Circulation 109, 2058-2067.
133. Verma, S., Devaraj, S., Jialal, I. (2006). C-reactive protein promotes atherothrombosis. Circulation 113, 2135-2151.
134. Vigo, C. (1985). Effect of C-reactive protein on platelet-activating factor-induced platelet aggregation and membrane stabilization. J. Biol. Chem. 260, 3418-3422.
135. Vigushin, D.M., Pepys, M.B., Hawkins, P.N. (1993). Metabolic and scintigraphic studies of raioiodinated human C-reactive protein in health and disease. J. Clin. Invest. 91, 1351-1357.
136. Vilahur, G., Herndez-Vera, R., Molins, B., Casani, L., Duran, X., Padr T., Badimon, L. (2009). Short-term myocardial ischemia induces cardiac modified C-reactive protein expression and proinflammatory gene (cyclo-oxygenase-2, monocyte chemoattractant protein-1, and tissue factor) upregulation in peripheral blood mononuclear cells. J. Thromb. Haemost. 7, 485-493.
137. Walsh, M.T., Divane, A., Whitehead, A.S. (1996). Fine mapping of the human pentraxin gene region on chromosome 1q23. Immunogenetics 44, 62-69.
138. Wang, H.W., Sui, S.F. (2001). Dissociation and subunit rearrangement of membrane-bound human C-reactive proteins. Biochem. Biophys. Res. Commun. 288, 75-79.
139. Wang, M.S., Black, J.C., Knowles, M.K., Reed, S.M. (2011a). C-reactive protein (CRP) aptamer binds to monomeric but not pentameric from of CRP. Anal. Bioanal. Chem. 401, 1309-1318.
140. Wang, M.-Y., Ji, S.-R., Bai, C.-J., El Kebir, D., Li, H.-Y., Shi, J.-M., Zhu, W., Costantino, S., Zhou, H.-H., Potempa, L.A., et al. (2011b). A redox switch in C-reactive protein modulates activation of endothelial cells. FASEB J. 25, 3186-3196.
141. Wang, M.S., Messersmith R.E., Reed, S.M. (2012). Membrane curvature recognition by C-reactive protein using lipoprotein mimics. Soft Matter 8, 7909-7918.
142. Wang, J., Tang, B., Liu, X., Wu, X., Wang, H., Xu, D., Guo, Y. (2015). Increased monomeric CRP levels in acute myocardial infarction: a possible new and specific biomarker for diagnosis and severity assessment of disease. Atherosclerosis 239, 343-349.
143. Xia, D., Samols, D. (1997). Transgenic mice expressing rabbit C-reactive protein are resistant to endotoxemia. Proc. Natl. Acad. Sci. USA 94, 2575-2580.
144. Yasojima, K., Schwab, C., McGeer, E.G., McGeer, P.L. (2001). Generation of C-reactive protein and complement components in atherosclerotic plaques. Am. J. Pathol. 158, 1039-1051.
145. Ying, S.-C., Gewurz, H., Kinoshita, C.M., Potempa, L.A., Siegel, J.N. (1989) Identification and partial characterization of multiple native and neoantigenic epitopes of human C-reactive protein. J. Immunol. 143, 221-228.
146. Ying, S.-C., Shephard, E., de Beer, F.C., Siegel, J.N., Harris, D., Gewurz, B.E., Friedkin, M., Gewurz, H. (1992). Localization of sequence-determined neoepitopes and neutrophil digestion fragments of C-reactive protein utilizing monoclonal antibodies and synthetic peptides. Mol. Immunol. 29, 677-687.
147. Zhong, W., Zen, Q., Tebo, J., Schlottmann, K., Coggeshall, M., Mortenson, R.F. (1998). Effect of human C-reactive protein on chemokine and chemotactic factor-induced neutrophil chemotaxis and signaling. J. Immunol. 161, 2533-2540.
148. Zhou, P., Thomassen, M.J., Pettay, J., Deodhar, S.D., Barna, B.P. (1995). Human monocytes produce monocyte chemoattractant protein 1 (MCP-1) in response to a synthetic peptide derived from C-reactive protein. Clin. Immunol. Immunopathol. 74, 84-88.
149. Zouki, C., Beauchamp, M., Baron, C., Filep, J.G. (1997). Prevention of in vitro neutrophil adhesion to endothelial cells through shedding of L-selectin by C-reactive protein and peptides derived from C-reactive protein. J. Clin. Invest. 100, 522-529.
150. Zouki, C., Haas, B., Chan, J.S.D., Potempa, L.A., Filep, J.G. (2001). Loss of pentameric symmetry of C-reactive protein is associated with promotion of neutrophil-endothelial cell adhesion. J. Immunol. 167, 5355-5361.
151. Zwaka, T.P., Hombach, V., Torzewski, J. (2001). C-reactive protein-mediated low density lipoprotein uptake by macrophages: implications for atherosclerosis. Circulation 103, 1194-1197.