Polyphosphate elicits pro-inflammatory responses that are counteracted by activated protein C in both cellular and animal models

Journal of Thrombosis and Haemostasis

Volumn 10, Issue 6, 2012, Pages 1145-1151

  Bae, J S ^a   Lee, W ^a,b   Rezaie, A R ^c  

^a Kyungpook National University   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell adhesion; Coagulation; Inflammation; Permeability; Polyphosphate; Signal transduction

Indexed keywords

ACTIVATED PROTEIN C; BOVINE SERUM ALBUMIN; CELL ADHESION MOLECULE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; POLYPHOSPHATE; PROCOAGULANT; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BLOOD CLOTTING; BLOOD VESSEL PERMEABILITY; CELL ADHESION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; EXTRAVASATION; HUMAN; HUMAN CELL; INFLAMMATION; LEUKOCYTE MIGRATION; MOUSE; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; APOPTOSIS; CAPILLARY PERMEABILITY; CELL ADHESION; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CHEMOTAXIS, LEUKOCYTE; COCULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; E-SELECTIN; FEMALE; HEPARIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INJECTIONS, INTRAPERITONEAL; INJECTIONS, INTRAVENOUS; INTERCELLULAR ADHESION MOLECULE-1; MICE; MICE, INBRED ICR; NF-KAPPA B; POLYPHOSPHATES; PROTEIN C; UP-REGULATION; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84861664297     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2012.04671.x     Document Type: Article

References (30)

1. Kumble KD, Kornberg A. Inorganic polyphosphate in mammalian cells and tissues. J Biol Chem 1995; 270: 5818-22.
2. Ruiz FA, Lea CR, Oldfield E, Docampo R. Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J Biol Chem 2004; 279: 44250-7.
3. Müller F, Mutch NJ, Schenk WA, Smith SA, Esterl L, Spronk HM, Schmidbauer S, Gahl WA, Morrissey JH, Renné T. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009; 139: 1143-56.
4. Smith SA, Morrissey JH. Polyphosphate as a general procoagulant agent. J Thromb Haemost 2008; 6: 1750-6.
5. Choi SH, Smith SA, Morrissey JH. Polyphosphate is a cofactor for the activation of factor XI by thrombin. Blood 2011; 118: 6963-70.
6. Mutch NJ, Myles T, Leung LL, Morrissey JH. Polyphosphate binds with high affinity to exosite II of thrombin. J Thromb Haemost 2010; 8: 548-55.
7. Smith SA, Choi SH, Davis-Harrison R, Huyck J, Boettcher J, Rienstra CM, Morrissey JH. Polyphosphate exerts differential effects on blood clotting, depending on polymer size. Blood 2010; 116: 4353-9.
8. Gettins PG, Olson ST. Exosite determinants of serpin specificity. J Biol Chem 2009; 284: 20441-5.
9. Gailani D, Broze GJ Jr. Factor XI activation in a revised model of blood coagulation. Science 1991; 253: 909-12.
10. Esmon CT. Inflammation and thrombosis. J Thromb Haemost 2003; 1: 1343-8.
11. Yang L, Manithody C, Rezaie AR. Contribution of basic residues of the 70-80-loop to heparin binding and anticoagulant function of activated protein C. Biochemistry 2002; 41: 6149-57.
12. Bae JS, Rezaie AR. Activated protein C inhibits high mobility group box 1 signaling in endothelial cells. Blood 2011; 118: 3952-9.
13. Bae JS, Yang L, Manithody C, Rezaie AR. Engineering a disulfide bond to stabilize the calcium-binding loop of activated protein C eliminates its anticoagulant but not its protective signaling properties. J Biol Chem 2007; 282: 9251-9.
14. Bae JS, Yang L, Manithody C, Rezaie AR. The ligand occupancy of endothelial protein C receptor switches the PAR-1-dependent signaling specificity of thrombin from a permeability-enhancing to a barrier-protective response in endothelial cells. Blood 2007; 110: 3909-16.
15. Lee JD, Huh JE, Jeon G, Yang HR, Woo HS, Choi DY, Park DS. Flavonol-rich RVHxR from Rhus verniciflua Stokes and its major compound fisetin inhibits inflammation-related cytokines and angiogenic factor in rheumatoid arthritic fibroblast-like synovial cells and in vivo models. Int Immunopharmacol 2009; 9: 268-76.
16. Han KY, Hong BS, Yoon YJ, Yoon CM, Kim YK, Kwon YG, Gho YS. Polyphosphate blocks tumour metastasis via anti-angiogenic activity. Biochem J 2007; 406: 49-55.
17. Lorenz B, Leuck J, Köhl D, Muller WE, Schröder HC. Anti-HIV-1 activity of inorganic polyphosphates. J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14: 110-8.
18. Smith SA, Mutch NJ, Baskar D, Rohloff P, Docampo R, Morrissey JH. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci U S A 2006; 103: 903-8.
19. Mosnier LO, Zlokovic BV, Griffin JH. The cytoprotective protein C pathway. Blood 2007; 109: 3161-72.
20. Rezaie AR. Rapid activation of protein C by factor Xa and thrombin in the presence of polyanionic compounds. Blood 1998; 91: 4572-80.
21. Nicolaes GA, Sørensen KW, Friedrich U, Tans G, Rosing J, Autin L, Dahlbäck B, Villoutreix BO. Altered inactivation pathway of factor Va by activated protein C in the presence of heparin. Eur J Biochem 2004; 271: 2724-36.
22. Young E. The anti-inflammatory effects of heparin and related compounds. Thromb Res 2008; 122: 743-52.
23. Gori AM, Attanasio M, Gazzini A, Rossi L, Lucarini L, Miletti S, Chini J, Manoni M, Abbate R, Gensini GF. Cytokine gene expression and production by human LPS-stimulated mononuclear cells are inhibited by sulfated heparin-like semi-synthetic derivatives. J Thromb Haemost 2004; 2: 1657-62.
24. Thourani VH, Brar SS, Kennedy TP, Thornton LR, Watts JA, Ronson RS, Zhao ZQ, Sturrock AL, Hoidal JR, Vinten-Johansen J. Nonanticoagulant heparin inhibits NF-kappaB activation and attenuates myocardial reperfusion injury. Am J Physiol Heart Circ Physiol 2000; 278: H2084-93.
25. Lin YZ, Yao SY, Veach RA, Torgerson TR, Hawiger J. Inhibition of nuclear translocation of transcription factor NF-kappa B by a synthetic peptide containing a cell membrane-permeable motif and nuclear localization sequence. J Biol Chem 1995; 270: 14255-8.
26. Shiba T, Nishimura D, Kawazoe Y, Onodera Y, Tsutsumi K, Nakamura R, Ohshiro M. Modulation of mitogenic activity of fibroblast growth factors by inorganic polyphosphate. J Biol Chem 2003; 278: 26788-92.
27. Kawazoe Y, Katoh S, Onodera Y, Kohgo T, Shindoh M, Shiba T. Activation of the FGF signaling pathway and subsequent induction of mesenchymal stem cell differentiation by inorganic polyphosphate. Int J Biol Sci 2008; 4: 37-47.
28. Segerer S, Johnson Z, Rek A, Baltus T, von Hundelshausen P, Kungl AJ, Proudfoot AE, Weber C, Nelson PJ. The basic residue cluster (55)KKWVR(59) in CCL5 is required for in vivo biologic function. Mol Immunol 2009; 46: 2533-8.
29. Severin IC, Gaudry JP, Johnson Z, Kungl A, Jansma A, Gesslbauer B, Mulloy B, Power C, Proudfoot AE, Handel T. Characterization of the chemokine CXCL11-heparin interaction suggests two different affinities for glycosaminoglycans. J Biol Chem 2010; 285: 17713-24.
30. Riewald M, Petrovan RJ, Donner A, Mueller BM, Ruf W. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science 2002; 296: 1880-2.