Binding of C-reactive protein to modified low-density-lipoprotein particles: Identification of cholesterol as a novel ligand for C-reactive protein

Biochemical Journal

Volumn 367, Issue 2, 2002, Pages 403-412

  Taskinen, Sanna ^a   Kovanen, Petri T ^a   Jarva, Hanna ^a   Meri, Seppo ^a   Pentikäinen, Markku O ^a  

^a WIHURI RESEARCH INSTITUTE   (Finland)

Author keywords

Atherosclerosis; Cholesterol; Inflammation

Indexed keywords

CHOLESTEROL; LIPIDS; MIXING; OXIDATION; PROTEINS;

LIPOLYSIS;

BIOCHEMISTRY;

ACUTE PHASE PROTEIN; C REACTIVE PROTEIN; CALCIUM ION; CHOLESTEROL; CHOLESTEROL ESTERASE; CHOLESTEROL OXIDASE; CYCLODEXTRIN; LIGAND; LIPID; LOW DENSITY LIPOPROTEIN; PHOSPHOLIPASE A; PHOSPHORYLCHOLINE; SPHINGOMYELIN PHOSPHODIESTERASE; TRYPSIN;

ACUTE PHASE RESPONSE; ARTERY INTIMA; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BINDING COMPETITION; BINDING KINETICS; CHEMICAL MODIFICATION; CHOLESTEROL ESTERIFICATION; CHOLESTEROL METABOLISM; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME BINDING; HUMAN; HUMAN CELL; INFLAMMATION; LIGAND BINDING; LIPOLYSIS; MOLECULAR INTERACTION; OXIDATION KINETICS; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; PROTEIN LIPID INTERACTION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; SURFACE CHARGE;

ARTERIOSCLEROSIS; C-REACTIVE PROTEIN; CALCIUM; CHOLESTEROL; CHOLESTEROL ESTERASE; CYCLODEXTRINS; HUMANS; LIGANDS; LIPOPROTEINS, LDL; OXIDATION-REDUCTION; PHOSPHATIDYLCHOLINES; PHOSPHOLIPASES A; SPHINGOMYELIN PHOSPHODIESTERASE; TRYPSIN;

EID: 0037108874     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20020492     Document Type: Article

References (52)

1. Ross, R. (1999) Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340, 115-126
2. Cushing, S. D., Berliner, J. A., Valente, A. J., Territo, M. C., Navab, M., Parhami, F., Gerrity, R., Schwartz, C. J. and Fogelman, A. M. (1990) Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. Proc. Natl. Acad. Sci. U.S.A. 87, 5134-5138
3. 2 in atherosclerosis. Atherosclerosis 132, 1-8
4. Klouche, M., May, A. E., Hemmes, M., Messner, M., Kanse, S. M., Preissner, K. T. and Bhakdi, S. (1999) Enzymatically modified, nonoxidized LDL induces selective adhesion and transmigration of monocytes and T-lymphocytes through human endothelial cell monolayers. Arterioscler. Thromb. Vasc. Biol. 19, 784-793
5. Klouche, M., Gottschling, S., Gerl, V., Hell, W., Husmann, M., Dorweiler, B., Messner, M. and Bhakdi, S. (1998) Atherogenic properties of enzymatically degraded LDL-Selective induction of MCP-1 and cytotoxic effects on human macrophages. Arterioscler. Thromb. Vasc. Biol. 18, 1376-1385
6. Shrive, A. K., Cheetham, G. M., Holden, D., Myles, D. A., Turnell, W. G., Volanakis, J. E., Pepys, M. B., Bloomer, A. C. and Greenhough, T. J. (1996) Three dimensional structure of human C-reactive protein. Nat. Struct. Biol. 3, 346-354
7. Volanakis, J. E. and Kaplan, M. H. (1971) Specificity of C-reactive protein for choline phosphate residues of pneumococcal C-polysaccharide. Proc. Soc Exp. Biol. Med. 136, 612-614
8. Volanakis, J. E. and Wirtz, K. W. (1979) Interaction of C-reactive protein with artificial phosphatidylcholine bilayers. Nature (London) 281, 155-157
9. Gershov, D., Kim, S., Brot, N. and Elkon, K. B. (2000) C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: Implications for systemic autoimmunity. J. Exp. Med. 192, 1353-1364
10. Salonen, E. M., Vartio, T. Hedman, K. and Vaheri, A. (1984) Binding of fibronectin by the acute phase reactant C-reactive protein. J. Biol. Chem. 259, 1496-1501
11. Robey, F. A., Jones, K. D., Tanaka, T. and Liu, T. Y. (1984) Binding of C-reactive protein to chromatin and nucleosome core particles. A possible physiological role of C-reactive protein. J. Biol. Chem. 259, 7311-7316
12. Du Clos, T. W. (1989) C-reactive protein reacts with the U1 small nuclear ribonucleoprotein. J. Immunol. 143, 2553-2559
13. DiCamelli, R., Potempa, L. A., Siegel, J., Suyehira, L., Petras, K. and Gewurz, H. (1980) Binding reactivity of C-reactive protein for polycations. J. Immunol. 125, 1933-1938
14. Claus, D. R., Siegel, J., Petras, K., Osmand, A. P. and Gewurz, H. (1977) Interactions of C-reactive protein with the first component of human complement. J. Immunol. 119, 187-192
15. Bharadwaj, D., Stein, M. P., Volzer, M., Mold, C. and Du Clos, T. W. (1999) The major receptor for C-reactive protein on leukocytes is fcgamma receptor II. J. Exp. Med. 190, 585-590
16. Kaplan, M. H. and Volanakis, J. E. (1974) Interaction of C-reactive protein complexes with the complement system I. Consumption of human complement associated with the reaction of C-reactive protein with pneumococcal C-polysaccharide and with the choline phosphatides, lecithin and sphingomyelin. J. Immunol. 112, 2135-2147
17. Jarva, H., Jokiranta, T. S., Hellwage, J., Zipfel, P. F. and Meri, S. (1999) Regulation of complement activation by C-reactive protein: Targeting the complement inhibitory activity of factor H by an interaction with short consensus repeat domains 7 and 8-11. J. Immunol. 163, 3957-3962
18. Vlaicu, R., Rus, H. G., Niculescu, F. and Cristea, A. (1985) Quantitative determinations of immunoglobulins and complement components in human aortic atherosclerotic wall. Med. Int. 23, 29-35
19. Reynolds, G. D. and Vance, R. P. (1987) C-reactive protein immunohistochemical localization in normal and atherosclerotic human aortas. Arch. Pathol. Lab. Med. 111, 265-269
20. Zhang, Y. X., Cliff, W. J., Schoefl, G. I. and Higgins, G. (1999) Coronary C-reactive protein distribution: Its relation to development of atherosclerosis. Atherosclerosis 145, 375-379
21. Torzewski, J., Torzewski, M., Bowyer, D. E., Frohlich, M., Koenig, W., Waltenberger, J., Fitzsimmons, C. and Hombach, 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
22. Rowe, I. F., Soutar, A. K., Trayner, I. M., Baltz, M. L., de Beer, F. C., Walker, L., Bowyer, D., Herbert, J., Feinstein, A. and Pepys, M. B. (1984) Rabbit and rat C-reactive proteins bind apolipoprotein B-containing lipoproteins. J. Exp. Med. 159, 604-616
23. Bhakdi, S., Torzewski, M., Klouche, M. and Hemmes, M. (1999) Complement and atherogenesis: Binding of CRP to degraded, nonoxidized LDL enhances complement activation. Arterioscler. Thromb. Vasc. Biol. 19, 2348-2354
24. Pentikäinen, M. O., Öömi, K., Ala-Korpela, M. and Kovanen, P. T. (2000) Modified LDL-trigger of atherosclerosis and inflammation in the arterial intima. J. Int. Med. 247, 359-370
25. Havel, R. J., Eder, H. A. and Bragdon, J. H. (1955) The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Clin. Invest. 34, 1345-1353
26. 125I-containing acylating agent. Biochem. J. 133, 529-539
27. 125I-labeled modified C-reactive protein in CD-1 mice. Drug Metab. Dispos. 26, 977-981
28. Öörni, K., Pentikäinen, M. O., Annila, A. and Kovanen, P. T. (1997) Oxidation of low density lipoprotein particles decreases their ability to bind to human aortic proteoglycans: Dependence on oxidative modification of the lysine residues. J. Biol. Chem. 272, 21303-21311
29. Pentikäinen, M. O., Öörni, K. and Kovanen, P. T. (2001) Myeloperoxidase and hypochlorite, but not copper ions, oxidize heparin-bound LDL particles and release them from heparin. Arterioscler. Thromb. Vasc. Biol. 21, 1902-1908
30. a Bligh, E. G. and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Phys. 37, 911-917
31. Slotte, J. P. and Gronberg, L. (1990) Oxidation of cholesterol in low density and high density lipoproteins by cholesterol oxidase. J. Lipid Res. 31, 2235-2242
32. Okamoto, Y., Ninomiya, H., Miwa, S. and Masaki, T. (2000) Cholesterol oxidation switches the internalization pathway of endothelin receptor type A from caveolae to clathrin-coated pits in Chinese hamster ovary cells. J. Biol. Chem. 275, 6439-6446
33. Yancey, P. G., Rodrigueza, W. V., Kilsdonk, E. P., Stoudt, G. W., Johnson, W. J., Phillips, M. C. and Rothblat, G. H. (1996) Cellular cholesterol efflux mediated by cyclodextrins. Demonstration of kinetic pools and mechanism of efflux. J. Biol. Chem. 271, 16026-16034
34. Chao, F. F., Blanchette-Mackie, E. J., Tertov, V. V., Skarlatos, S. I., Chen, Y. J. and Kruth, H. S. (1992) Hydrolysis of cholesteryl ester in low density lipoprotein converts this lipoprotein to a liposome. J. Biol. Chem. 267, 4992-4998
35. Bhakdi, S., Dorweiler, B., Kirchmann, R., Torzewski, J., Weise, E., Tranum, J., Walev, I. and Wieland, E. (1995) On the pathogenesis of atherosclerosis: Enzymatic transformation of human low density lipoprotein to an atherogenic moiety. J. Exp. Med. 182, 1959-1971
36. Pentikäinen, M. O., Lehtonen, E. M. P. and Kovanen, P. T. (1996) Aggregation and fusion of modified low density lipoprotein. J. Lipid Res. 37, 2638-2649
37. Hevonoja, T., Pentikäinen, M. O., Hyvönen, M. T., Kovanen, P. T. and Ala-Korpela, M. (2000) Structure of low density lipoprotein (LDL) particles. Basis for understanding molecular changes in modified LDL. Biochim. Biophys. Acta 1488, 189-210
38. Irie, T., Fukunaga, K. and Pitha, J. (1992) Hydroxypropylcyclodextrins in parenteral use. I: Lipid dissolution and effects on lipid transfers in vitro. J. Pharm. Sci. 81, 521-523
39. Tillett, W. S. and Francis, T. (1930) Serological reactions in pneumonia with non-protein fraction of pneumococcus. J. Exp. Med. 52, 561-571
40. Harnett, W. and Harnett, M. M. (1999) Phosphocholine: Friend or foe of the immune system? Immunol. Today 20, 125-129
41. Kres, J. J. Potempa, L. A. and 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
42. de Beer, F. C., Soutar, A. K., Baltz, M. L., Trayner, I. M., Feinstein, A. and Pepys, M. B. (1982) Low density lipoprotein and very low density lipoprotein are selectively bound by aggregated C-reactive protein. J. Exp. Med. 156, 230-242
43. Rees, R. F., Gewurz, H., Siegel, J. N., Coon, J. and Potempa, L. A. (1988) Expression of a C-reactive protein neoantigen (neo-CRP) in inflamed rabbit liver and muscle Clin. Immunol Immunopathol. 48, 95-107
44. Zwaka, T. P., Hombach, V. and Torzewski, J. (2001) C-reactive protein-mediated low density lipoprotein uptake by macrophages: Implications for atherosclerosis. Circulation 103, 1194-1197
45. Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M. and Green, D. R. (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: Inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182, 1545-1556
46. 2 to liberate arachidonic acid. Biochim. Biophys. Acta 1349, 43-54
47. 2 in human atherosclerotic plaques. Atherosclerosis 118, 173-181
48. A induces particle fusion and enhances retention of LDL to human aortic proteoglycans. Arterioscler. Thromb. Vasc. Biol. 21, 1053-1058
49. 2+-dependent binding of rabbit C-reactive protein to supported lipid monolayers containing exposed phosphocholine group. Biophys. J. 76, 333-341
50. Tulenko, T. N., Chen, M., Mason, P. E. and Mason, R. P. (1998) Physical effects of cholesterol on arterial smooth muscle membranes: Evidence of immiscible cholesterol domains and alterations in bilayer width during atherogenesis J. Lipid Res. 39, 947-956
51. Kruth, H. S., Ifrim, I., Chang, J., Addadi, L., Perl-Treves, D. and Zhang, W. Y. (2001) Monoclonal antibody detection of plasma membrane cholesterol microdomains responsive to cholesterol trafficking. J. Lipid Res. 42, 1492-1500
52. Griselli, M., Herbert, J., Hutchinson, W. L., Taylor, K. M., Sohail, M., Krausz, T. and 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