C-reactive protein-derived peptide 201-206 inhibits neutrophil adhesion to endothelial cells and platelets through CD32

Journal of Leukocyte Biology

Volumn 90, Issue 6, 2011, Pages 1167-1175

  El Kebir, Driss ^a   Zhang, Ying ^a   Potempa, Lawrence A ^b   Wu, Yi ^c   Fournier, Alain ^d   Filep, János G ^a  

^a UNIVERSITY OF MONTREAL   (Canada)

^b ROOSEVELT UNIVERSITY   (United States)

^c LANZHOU UNIVERSITY   (China)

^d INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

Cell adherence; Fc ; Inflammation; Mutated CRP peptides; Receptors; Selectins

Indexed keywords

AMINO ACID; C REACTIVE PROTEIN; CD32 ANTIGEN; L SELECTIN; LYSINE; PADGEM PROTEIN; PROLINE; TUMOR NECROSIS FACTOR ALPHA;

AMINO ACID SUBSTITUTION; ARTICLE; CELL ADHESION; CELL INTERACTION; CONTROLLED STUDY; CORONARY ARTERY DISEASE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBOCYTE; UPREGULATION;

AMINO ACID SUBSTITUTION; BLOOD PLATELETS; C-REACTIVE PROTEIN; CELL ADHESION; CELLS, CULTURED; CORONARY THROMBOSIS; ENDOTHELIAL CELLS; HUMANS; NEUTROPHILS; PEPTIDE FRAGMENTS; RECEPTORS, IGG;

EID: 82555193652     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0111032     Document Type: Article

References (49)

1. Gabay, C., Kushner, I. (1999) Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 340, 448-454.
2. Black, S., Kushner, I., Samols, D. (2004) C-reactive protein. J. Biol. Chem. 279, 48487-48490.
3. Pepys, M. B., Hirschfield, G. M. (2003) C-reactive protein: a critical update. J. Clin. Invest. 111, 1805-1812.
4. Marnell, L. L., Mold, C., Volzer, M. A., Burlingame, R. W., Du Clos, T. W. (1995) C-reactive protein binds to FcγRI in transfected COS cells. J. Immunol. 155, 2185-2193.
5. 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 Fcγ receptor II. J. Exp. Med. 190, 585-590.
6. Xia, D., Samols, D. (1997) Transgenic mice expressing rabbit C-reactive protein are resistant to endotoxemia. Proc. Natl. Acad. Sci. USA 94, 2575-2580.
7. 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.
8. Verma, S., Devaraj, S., Jialal, I. (2006) C-reactive protein promotes atherothrombosis. Circulation 113, 2135-2150.
9. Singh, S. K., Suresh, M. V., Voleti, B., Agrawal, A. (2008) The connection between C-reactive protein and atherosclerosis. Ann. Med. 40, 110-120.
10. 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.
11. Filep, J. G. (2009) Platelets affect the structure and function of C-reactive protein. Circ. Res. 105, 109-111.
12. Perkins, S. J., Okemefuna, A. I., Nan, R. (2010) Unraveling protein-protein interactions between complement factor H and C-reactive protein using a multidisciplinary strategy. Biochem. Soc. Trans. 38, 894-900.
13. Hammond, D. J., 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.
14. 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.
15. 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., Chin-Dusting, J., Bobik, A., Peter, K. (2009) Dissociation of pentameric to monomeric C-reactive protein on activated platelets localizes inflammation to atherosclerotic plaques. Circ. Res. 105, 128-137.
16. Khreiss, T., József, L., Potempa, L. A., Filep, J. G. (2005) Loss of pentameric symmetry in C-reactive protein induces interleukin-8 secretion through peroxynitrite signaling in human neutrophils. Circ. Res. 97, 690-697.
17. Khreiss, T., József, L., Potempa, L. A., Filep, J. G. (2004) Opposing effects of C-reactive protein isoforms on shear-induced neutrophil-platelet adhesion and neutrophil aggregation in whole blood. Circulation 110, 2713-2720.
18. Molins, B., Pena, 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.
19. 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., Zhao, J., Filep, J. G., Wu, Y. (2011) A redox switch in C-reactive protein modulates activation of endothelial cells. FASEB J. 25, 3186-3196.
20. 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.
21. 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 FcγRI, FcγRIIA, and C1q by site-directed mutagenesis. J. Biol. Chem. 280, 25095-25102.
22. Agrawal, A., Volanakis, J. E. (1994) Probing the binding site on human C-reactive protein by site-directed mutagenesis. J. Immunol. 152, 5404-5410.
23. Shephard, E. G., Anderson, 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.
24. Heuertz, R. M., Ahmed, N., Webster, R. O. (1996) Peptides derived from C-reactive protein inhibit neutrophil alveolitis. J. Immunol. 156, 3412-3417.
25. 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.
26. 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.
27. Lu, J., Marnell, L. L., Marjon, K. D., Mold, C., Du Clos, T. W., Sun, P. D. (2008) Structural recognition and functional activation of FcγR by innate pentraxins. Nature 456, 989-992.
28. Finn, A. V., Nakano, M., Narula, J., Kolodgie, F. D., Virmani, R. (2010) Concept of vulnerable/unstable plaque. Arterioscler. Thromb. Vasc. Biol. 30, 1282-1292.
29. Walcheck, B., Kahn, J., Fisher, J. M., Wang, B. B., Fisk, R. S., Payan, D. G., Feehan, C., Betageri, R., Darlak, K., Spatola, A. F., Kishimoto, T. K. (1996) Neutrophil rolling altered by inhibition of L-selectin shedding in vitro. Nature 380, 720-723.
30. Khreiss, T., József, L., Potempa, L. A., Filep, J. G. (2004) Conformational rearrangement in C-reactive protein is required for proinflammatory actions on human endothelial cells. Circulation 109, 2016-2022.
31. Bunk, S., Sigel, S., Metzdorf, D., Sharif, O., Triantafilou, K., Triantafilou, M., Hartung, T., Knapp, S., von Aulock, S. (2010) Internalization and co-receptor expression are critical for TLR2-mediated recognition of lipoteichoic acid in human peripheral blood. J. Immunol. 185, 3708-3717.
32. Konstantopoulos, K., Neelanegham, S., Burns, A. R., Hentzen, E., Kansas, G. S., Snapp, K. R., Berg, E. L., Hellums, J. D., Smith, C. W., McIntire, L. V., Simon, S. I. (1998) Venous levels of shear support neutrophil-platelet adhesion and neutrophil aggregation in blood via P-selectin and β2- integrin. Circulation 98, 873-882.
33. Taylor, A. D., Neelamegham, S., Hellums, J. D., Smith, C. W., Simon, S. I. (1996) Molecular dynamics of the transition from L-selectin to β2-integrin-dependent neutrophil adhesion under defined hydrodynamic shear. Biophys. J. 71, 3488-3500.
34. 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.
35. 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.
36. Walcheck, B., Alexander, S. R., St Hill, C. A., Matala, E. (2003) ADAM-17-independent shedding of L-selectin. J. Leukoc. Biol. 74, 389-394.
37. Bennett, T. A., Lynam, E. B., Sklar, L. A., Rogelj, S. (1996) Hydroxamatebased metalloprotease inhibitor blocks shedding of L-selectin adhesion molecule from leukocytes: functional consequences for neutrophil aggregation. J. Immunol. 156, 3093-3097.
38. Diacovo, T. G., Roth, S. J., Buccola, J. M., Bainton, D. F., Springer, T. A. (1996) Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the β 2-integrin Mac-1 (CD11b/CD18). Blood 88, 146-157.
39. Devaraj, S., Du Clos, T. W., Jialal, I. (2005) Binding and internalization of C-reactive protein by Fc γ receptors on human aortic endothelial cells mediates biological effects. Arterioscler. Thromb. Vasc. Biol. 25, 1359-1363.
40. 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.
41. 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 micro-domains. FASEB J. 23, 1806-1816.
42. Nimmerjahn, F., Ravetch, J. V. (2008) Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47.
43. Huang, M. M., Indik, Z., Brass, L. F., Hoxie, J. A., Schreiber, A. D., Brugge, J. S. (1992) Activation of Fc γ RII induces tyrosine phosphorylation of multiple proteins including Fc γ RII. J. Biol. Chem. 267, 5467-5473.
44. Fitzgerald, J. R., Foster, T. J., Cox, D. (2006) The interaction of bacterial pathogens with platelets. Nat. Rev. Microbiol. 4, 445-457.
45. Brennan, M. P., Moriarty, R. D., Grennan, S., Chubb, A. J., Cox, D. (2008) C-reactive protein binds to αIIbβ3. J. Thromb. Haemost. 6, 1239-1241.
46. 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.
47. 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 infracted myocardium. J. Clin. Pathol. 58, 382-388.
48. 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.
49. Torzewski, M., Rist, C., Mortensen, R. F., Zwaka, T. P., Bienek, M., Waltenberger, J., Konig, 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.