Transitional changes in the CRP structure lead to the exposure of proinflammatory binding sites

Nature Communications

Volumn 8, Issue , 2017, Pages

  Braig, David ^a,b   Nero, Tracy L ^c   Koch, Hans Georg ^d   Kaiser, Benedict ^a   Wang, Xiaowei ^b,e   Thiele, Jan R ^a   Morton, Craig J ^c   Zeller, Johannes ^a   Kiefer, Jurij ^a   Potempa, Lawrence A ^f   Mellett, Natalie A ^b   Miles, Luke A ^c,g   Du, Xiao Jun ^b,e   Meikle, Peter J ^b,g   Huber Lang, Markus ^h   Stark, G Björn ^a   Parker, Michael W ^c,g   Peter, Karlheinz ^b,e   Eisenhardt, Steffen U ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^c ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF FREIBURG   (Germany)

^e MONASH UNIVERSITY   (Australia)

^f ROOSEVELT UNIVERSITY   (United States)

^g UNIVERSITY OF MELBOURNE   (Australia)

^h UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; COMPLEMENT FACTOR 1Q; COMPLEMENT FACTOR I; PHOSPHORYLCHOLINE; UNCLASSIFIED DRUG; 1,6-BIS(PHOSPHOCHOLINE)-HEXANE; HEXANE; LIPOPOLYSACCHARIDE; PROTEIN BINDING;

CELLS AND CELL COMPONENTS; CONCENTRATION (COMPOSITION); INFECTIVITY; INHIBITOR; INJURY; MUSCLE; PROTEIN;

ARTICLE; BINDING SITE; COMPLEMENT CLASSICAL PATHWAY; COMPLEMENT FIXATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; INFLAMMATION; LEUKOCYTE; MEMBRANE MICROPARTICLE; MONOCYTE; PROTEIN STRUCTURE; TISSUE INJURY; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY; PROTEIN CONFORMATION; RAT; SKELETAL MUSCLE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; C-REACTIVE PROTEIN; GENE EXPRESSION REGULATION; HEXANES; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MODELS, MOLECULAR; MONOCYTES; MUSCLE, SKELETAL; PHOSPHORYLCHOLINE; PROTEIN BINDING; PROTEIN CONFORMATION; RATS;

EID: 85010392563     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14188     Document Type: Article

References (69)

1. Volanakis, J. E. Human C-reactive protein: expression, structure, and function. Mol. Immunol. 38, 189-197 (2001).
2. Gill, R., Kemp, J. A., Sabin, C., Pepys, M. B. Human C-reactive protein increases cerebral infarct size after middle cerebral artery occlusion in adult rats. J. Cerebr. Blood Flow Metab. 24, 1214-1218 (2004).
3. Lane, T., et al. Infusion of pharmaceutical grade natural human C reactive protein is not pro inflammatory in healthy adult human volunteers. Circ. Res. 114, 672-676 (2013).
4. Thiele, J. R., et al. Dissociation of pentameric to monomeric C-reactive protein localizes and aggravates inflammation: in vivo proof of a powerful proinflammatory mechanism and a new anti-inflammatory strategy. Circulation 130, 35-50 (2014).
5. Griselli, M., et al. C-reactive protein and complement are important mediators of tissue damage in acute myocardial infarction. J. Exp Med. 190, 1733-1740 (1999).
6. Agrawal, A., Gang, T. B., Rusinol, A. E. Recognition functions of pentameric C-reactive protein in cardiovascular disease. Mediat. Inflamm. 2014, 319215 (2014).
7. Thompson, D., Pepys, M. B., Wood, S. P. The physiological structure of human C-reactive protein and its complex with phosphocholine. Structure 7, 169-177 (1999).
8. Lu, J., et al. Structural recognition and functional activation of FcgammaR by innate pentraxins. Nature 456, 989-992 (2008).
9. Singh, S. K., et al. Exposing a hidden functional site of C-reactive protein by site-directed mutagenesis. J. Biol. Chem. 287, 3550-3558 (2012).
10. Volanakis, J. E., Narkates, A. J. Interaction of C-reactive protein with artificial phosphatidylcholine bilayers and complement. J. Immunol. 126, 1820-1825 (1981).
11. Chang, M. K., Binder, C. J., Torzewski, M., Witztum, J. L. 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 (2002).
12. Agrawal, A., Shrive, A. K., Greenhough, T. J., Volanakis, J. E. Topology and structure of the C1q-binding site on C-reactive protein. J. Immunol. 166, 3998-4004 (2001).
13. Ji, S. R., et al. Cell membranes and liposomes dissociate C-reactive protein (CRP) to form a new, biologically active structural intermediate: mCRP(m). FASEB J. 21, 284-294 (2007).
14. Mihlan, M., et al. Monomeric C-reactive protein modulates classic complement activation on necrotic cells. FASEB J. 25, 4198-4210 (2011).
15. Braig, D., et al. A conformational change of C-reactive protein in burn wounds unmasks its proinflammatory properties. Int. Immunol. 26, 467-478 (2014).
16. Eisenhardt, S. U., et al. Dissociation of pentameric to monomeric C-reactive protein on activated platelets localizes inflammation to atherosclerotic plaques. Circ. Res. 105, 128-137 (2009).
17. Strang, F., et al. Amyloid plaques dissociate pentameric to monomeric C-reactive protein: a novel pathomechanism driving cortical inflammation in Alzheimer's disease? Brain Pathol. 22, 337-346 (2012).
18. Yang, X. W., Tan, Y., Yu, F., Zhao, M. H. Interference of antimodified C-reactive protein autoantibodies from lupus nephritis in the biofunctions of modified C-reactive protein. Hum. Immunol. 73, 156-163 (2012).
19. Slevin, M., et al. Modified C-reactive protein is expressed by stroke neovessels and is a potent activator of angiogenesis in vitro. Brain Pathol. 20, 151-165 (2010).
20. Pepys, M. B., et al. Targeting C-reactive protein for the treatment of cardiovascular disease. Nature 440, 1217-1221 (2006).
21. Buzas, E. I., Gyorgy, B., Nagy, G., Falus, A., Gay, S. Emerging role of extracellular vesicles in inflammatory diseases. Nat. Rev. Rheumatol. 10, 356-364 (2014).
22. Hugel, B., Martinez, M. C., Kunzelmann, C., Freyssinet, J. M. Membrane microparticles: two sides of the coin. Physiology 20, 22-27 (2005).
23. Jayachandran, M., Miller, V. M., Heit, J. A., Owen, W. G. Methodology for isolation, identification and characterization of microvesicles in peripheral blood. J. Immunol. Methods 375, 207-214 (2012).
24. Volanakis, J. E., Wirtz, K. W. Interaction of C-reactive protein with artificial phosphatidylcholine bilayers. Nature 281, 155-157 (1979).
25. Habersberger, J., et al. Circulating microparticles generate and transport monomeric C-reactive protein in patients with myocardial infarction. Cardiovasc. Res. 96, 64-72 (2012).
26. Shi, P., et al. Immunohistochemical staining reveals C-reactive protein existing predominantly as altered conformation forms in inflammatory lesions. Acta Biol. Hungar. 65, 265-273 (2014).
27. Wang, M. Y., et al. A redox switch in C-reactive protein modulates activation of endothelial cells. FASEB J. 25, 3186-3196 (2011).
28. Taylor, K. E., van den Berg, C. W. Structural and functional comparison of native pentameric, denatured monomeric and biotinylated C-reactive protein. Immunology 120, 404-411 (2007).
29. Pepys, M. B., et al. Isolation and characterization of pharmaceutical grade human pentraxins, serum amyloid P component and C-reactive protein, for clinical use. J. Immunol. Methods 384, 92-102 (2012).
30. Wang, J. G., et al. Monocytic microparticles activate endothelial cells in an IL-1beta-dependent manner. Blood 118, 2366-2374 (2011).
31. Zouki, C., Haas, B., Chan, J. S., Potempa, L. A., Filep, J. G. Loss of pentameric symmetry of C-reactive protein is associated with promotion of neutrophilendothelial cell adhesion. J. Immunol. 167, 5355-5361 (2001).
32. Li, H. Y., et al. Topological localization of monomeric C-reactive protein determines proinflammatory endothelial cell responses. J. Biol. Chem. 289, 14283-14290 (2014).
33. Motie, M., Schaul, K. W., Potempa, L. A. Biodistribution and clearance of 125I-labeled C-reactive protein and 125I-labeled modified C-reactive protein in CD-1 mice. Drug Metab. Dispos. 26, 977-981 (1998).
34. Christopeit, T., Gossas, T., Danielson, U. H. Characterization of Ca2 and phosphocholine interactions with C-reactive protein using a surface plasmon resonance biosensor. Anal. Biochetn. 391, 39-44 (2009).
35. Milcolajek, H., et al. Structural basis of ligand specificity in the human pentraxins, C-reactive protein and serum amyloid P component. J. Mol. Recogn. 24, 371-377 (2011).
36. Ji, S. R., et al. Monomeric C-reactive protein activates endothelial cells via interaction with lipid raft microdomains. FASEB J. 23, 1806 1816 (2009).
37. Bigay, J., Antonny, B. Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dcv. Cell 23, 886-895 (2012).
38. Mouritsen, 0. G. Lipids, curvature, and nano-medicine. Eur. I. Lipid Sci. Technol. 113, 1174-1187 (2011).
39. Wang, M. S., Messersmith, R. E., Reed, S. M. Membrane curvature recognition by C-reactive protein using lipoprotein mimics. Soft Matter 8, 7909-7918 (2012).
40. Pace, C. N., Grimsley, G. R., Scholtz, J. M. Protein ionizable groups: pKvalues and their contribution to protein stability and solubility. J. Biol. Chetn. 284, 13285-13289 (2009).
41. Hammond, Jr D. J., et al. Identification of acidic pH-dependent ligands of pentameric C-reactive protein. J. Biol. Chem. 285, 36235-36244 (2010).
42. Silver, I. A., Murrills, R. J., Etherington, D. J. Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Exp. Cell Res. 175, 266-276 (1988).
43. Sharpe, J. R., et al. Progression of wound pH during the course of healing in burns. J. Burn Care Res. 34, e201-e208 (2013).
44. Schneider, L. A., Korber, A., Grabbe, S., Dissemond, J. Influence of pH on wound-healing: a new perspective for wound-therapy? Arch. Dermatol. Res. 298, 413-420 (2007).
45. Ohkuma, S., Poole, B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. NatI Acad Sci USA 75, 3327-3331 (1978).
46. Leake, D. S. Does an acidic pH explain why low density lipoprotein is oxidised in atherosclerotic lesions? Atherosclerosis 129, 149-157 (1997).
47. Gaboriaud, C., et al. The crystal structure of the globular head of complement protein Clq provides a basis for its versatile recognition properties. J. Biol. Chem. 278, 46974-46982 (2003).
48. Roumenina, L. T., et al. Interaction of Clq with IgGl, C-reactive protein and pentraxin 3: mutational studies using recombinant globular head modules of human Clq A, B, and C chains. Biochemistry 45, 4093-4104 (2006).
49. Bang, R., et al. Analysis of binding sites in human C-reactive protein for Fc{gamma}RI, Fc{gamma}RIIA, and Clq by site-directed mutagenesis. J. Biol. Chem. 280, 25095-25102 (2005).
50. Gershov, D., Kim, S., Brot, N., Elkon, K. B. 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 (2000).
51. Poon, I. K., Lucas, C. D., Rossi, A. G., Ravichandran, K. S. Apoptotic cell clearance: basic biology and therapeutic potential. NaL Rev. ImmunoL 14, 166-180 (2014).
52. Agrawal, A. Not only immunoglobulins, C-reactive protein too. Mol. Immunol. 56, 561-562 (2013).
53. Xia, D., Samols, D. Transgenic mice expressing rabbit C-reactive protein are resistant to endotoxemia. Proc. NatI Acad. Sci. USA 94, 2575-2580 (1997).
54. Mold, C., Rodriguez, W., Rodic-Polic, B., Du Cbs, T. W. C-reactive protein mediates protection from lipopolysaccharide through interactions with Fc gamma R. J. Immunol. 169, 7019-7025 (2002).
55. Ward, N. S., Casserly, B., Ayala, A. The compensatory anti-inflammatory response syndrome (CARS) in critically ill patients. Clin. Chest Med. 29, 617-625 viii (2008).
56. Potempa, L. A., Siegel, J. N., Fiedel, B. A., Potempa, R. T., Gewurz, H. Expression, detection and assay of a neoantigen (Neo-CRP) associated with a free, human C-reactive protein subunit. Mol. Immunol. 24, 531-541 (1987).
57. Potempa, L. A., Yao, Z. Y., Ji, S. R., Filep, J. G., Wu, Y. Solubiization and purification of recombinant modified C-reactive protein from inclusion bodies using reversible anhydride modification. Biophys. Rep. 1, 18-33 (2015).
58. Ying, S. C., Gewurz, H., Kinoshita, C. M., Potempa, L. A., Siegel, J. N. Identification and partial characterization of multiple native and neoantigenic epitopes of human C-reactive protein by using monoclonal antibodies. J. Immunol. 143, 221-228 (1989).
59. Thiele, J. R., Goerendt, K., Stark, G. B., Eisenhardt, S. U. Real-time digital imaging of leukocyte-endothelial interaction in ischemia-reperfusion injury (IRI) of the rat cremaster muscle. J. Visual. Exp. 66, e3973 (2012).
60. Swamy, M., Siegers, G. M., Minguet, S., Wollscheid, B., Schamel, W. W. Blue native polyacrylamide gel electrophoresis (BN-PAGE) for the identification and analysis of multiprotein complexes. Sci. STKE 2006, p14 (2006).
61. Diehl, P., et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc. Res. 93, 633-644 (2012).
62. Nauseef, W. M. Isolation of human neutrophils from venous blood. Methods Mol. Biol. 1124, 13-18 (2014).
63. Braig, D., Bar, C., Thumfart, J. 0., Koch, H. G. Two cooperating helices constitute the lipid-binding domain of the bacterial SRP receptor. J. Mol. Biol. 390, 401-413 (2009).
64. Meilcle, P. J., et al. Plasma lipidomic analysis of stable and unstable coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 31, 2723-2732 (2011).
65. Weir, J. M., et al. Plasma lipid profiling in a large population-based cohort. J. Lipid Res. 54, 2898-2908 (2013).
66. Schmittgen, T. D., Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. NaL Protocols 3, 1101-1108 (2008).
67. Hong, C., Tieleman, D. P., Wang, Y. Microsecond molecular dynamics simulations of lipid mixing. Langmuir 30, 11993-12001 (2014).
68. Tan, K. P., Nguyen, T. B., Patel, S., Varadarajan, R., Madhusudhan, M. S. Depth: a web server to compute depth, cavity sizes, detect potential small-molecule ligand-binding cavities and predict the pKa of ionizable residues in proteins. Nucleic Acids Res. 41, W314-W321 (2013).
69. Lehrer, S. S. Solute perturbation of protein fluorescence. The quenching of the tryptophyl fluorescence of model compounds and of lysozyme by iodide ion. Biochemistry 10, 3254-3263 (1971).