Thrombin and activated protein C inhibit the expression of secretory group IIA phospholipase A2 in the TNF-α-activated endothelial cells by EPCR and PAR-1 dependent mechanisms

Thrombosis Research

Volumn 125, Issue 1, 2010, Pages e9-

  Bae, Jong Sup ^a   Rezaie, Alireza R ^b  

^a Daegu Haany University   (South Korea)

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

Author keywords

APC; HUVEC; Inflammation; PAR 1; PI3 kinase; Thrombin

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CHOLESTEROL; ENZYME PRECURSOR; METHYL BETA CYCLODEXTRIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE A2 GROUP II; PROTEIN C; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CONTROLLED STUDY; EMBRYO CELL; ENDOTHELIUM CELL; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INFLAMMATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 76449085291     PISSN: 00493848     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.thromres.2009.07.015     Document Type: Article

References (48)

1. Six D.A., and Dennis E.A. The expanding superfamily of phospholipase A(2) enzymes: classification and characterization. Biochim Biophys Acta 1488 (2000) 1-19
2. Kudo I., and Murakami M. Phospholipase A2 enzymes. Prostaglandins Other Lipid Mediat 68-69 (2002) 3-58
3. Chang H.W., Kudo I., Tomita M., and Inoue K. Purification and characterization of extracellular phospholipase A2 from peritoneal cavity of caseinate-treated rat. J Biochem 102 (1987) 147-154
4. Kramer R.M., Hession C., Johansen B., Hayes G., McGray P., Chow E.P., et al. Structure and properties of a human non-pancreatic phospholipase A2. J Biol Chem 264 (1989) 5768-5775
5. Seilhamer J.J., Pruzanski W., Vadas P., Plant S., Miller J.A., Kloss J., et al. Cloning and recombinant expression of phospholipase A2 present in rheumatoid arthritic synovial fluid. J Biol Chem 264 (1989) 5335-5338
6. Murakami M., Shimbara S., Kambe T., Kuwata H., Winstead M.V., Tischfield J.A., et al. The functions of five distinct mammalian phospholipase A2S in regulating arachidonic acid release. Type IIa and type V secretory phospholipase A2S are functionally redundant and act in concert with cytosolic phospholipase A2. J Biol Chem 273 (1998) 14411-14423
7. Menschikowski M., Hagelgans A., and Siegert G. Secretory phospholipase A2 of group IIA: is it an offensive or a defensive player during atherosclerosis and other inflammatory diseases?. Prostaglandins Other Lipid Mediat 79 (2006) 1-33
8. Mounier C.M., Hackeng T.M., Schaeffer F., Faure G., Bon C., and Griffin J.H. Inhibition of prothrombinase by human secretory phospholipase A2 involves binding to factor Xa. J Biol Chem 273 (1998) 23764-23772
9. Vadas P., and Pruzanski W. Role of secretory phospholipases A2 in the pathobiology of disease. Lab Invest 55 (1986) 391-404
10. Pruzanski W., and Vadas P. Phospholipase A2-a mediator between proximal and distal effectors of inflammation. Immunol Today 12 (1991) 143-146
11. Waydhas C., Nast-Kolb D., Duswald K.H., Lehnert P., and Schweiberer L. Prognostic value of serum phospholipase A in the multitraumatized patient. Klin Wochenschr 67 (1989) 203-206
12. Pruzanski W., Vadas P., Stefanski E., and Urowitz M.B. Phospholipase A2 activity in sera and synovial fluids in rheumatoid arthritis and osteoarthritis. Its possible role as a proinflammatory enzyme. J Rheumatol 12 (1985) 211-216
13. Vadas P., Browning J., Edelson J., and Pruzanski W. Extracellular phospholipase A2 expression and inflammation: the relationship with associated disease states. J Lipid Mediat 8 (1993) 1-30
14. Tanaka K., Kato T., Matsumoto K., and Yoshida T. Antiinflammatory action of thielocin A1 beta, a group II phospholipase A2 specific inhibitor, in rat carrageenan-induced pleurisy. Inflammation 17 (1993) 107-119
15. Murakami M., Nakatani Y., Atsumi G., Inoue K., and Kudo I. Regulatory functions of phospholipase A2. Crit Rev Immunol 17 (1997) 225-283
16. Joyce D.E., Gelbert L., Ciaccia A., DeHoff B., and Grinnell B.W. Gene expression profile of antithrombotic protein c defines new mechanisms modulating inflammation and apoptosis. J Biol Chem 276 (2001) 11199-11203
17. Mosnier L.O., Zlokovic B.V., and Griffin J.H. The cytoprotective protein C pathway. Blood 109 (2007) 3161-3172
18. Esmon C.T. Molecular events that control the protein C anticoagulant pathway. Thromb Haemost 70 (1993) 29-35
19. Bernard G.R., Vincent J.L., Laterre P.F., LaRosa S.P., Dhainaut J.F., Lopez-Rodriguez A., et al. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 344 (2001) 699-709
20. Riewald M., Petrovan R.J., Donner A., Mueller B.M., and Ruf W. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science 296 (2002) 1880-1882
21. Uchiba M., Okajima K., Oike Y., Ito Y., Fukudome K., Isobe H., et al. Activated protein C induces endothelial cell proliferation by mitogen-activated protein kinase activation in vitro and angiogenesis in vivo. Circ Res 95 (2004) 34-41
22. Xue M., Campbell D., Sambrook P.N., Fukudome K., and Jackson C.J. Endothelial protein C receptor and protease-activated receptor-1 mediate induction of a wound-healing phenotype in human keratinocytes by activated protein C. J Invest Dermatol 125 (2005) 1279-1285
23. Bretschneider E., Uzonyi B., Weber A.A., Fischer J.W., Pape R., Lotzer K., et al. Human vascular smooth muscle cells express functionally active endothelial cell protein C receptor. Circ Res 100 (2007) 255-262
24. Garcia J.G., Pavalko F.M., and Patterson C.E. Vascular endothelial cell activation and permeability responses to thrombin. Blood Coagul Fibrinolysis 6 (1995) 609-626
25. Finigan J.H., Dudek S.M., Singleton P.A., Chiang E.T., Jacobson J.R., Camp S.M., et al. Activated protein C mediates novel lung endothelial barrier enhancement: role of sphingosine 1-phosphate receptor transactivation. J Biol Chem 280 (2005) 17286-17293
26. Bae J.S., and Rezaie A.R. Protease activated receptor 1 (PAR-1) activation by thrombin is protective in human pulmonary artery endothelial cells if endothelial protein C receptor is occupied by its natural ligand. Thromb Haemost 100 (2008) 101-109
27. Bae J.S., and Rezaie A.R. Thrombin inhibits nuclear factor kappaB and RhoA pathways in cytokine-stimulated vascular endothelial cells when EPCR is occupied by protein C. Thromb Haemost 101 (2009) 513-520
28. Bae J.S., Yang L., Manithody C., and Rezaie A.R. The ligand occupancy of endothelial protein C receptor switches the protease-activated receptor 1-dependent signaling specificity of thrombin from a permeability-enhancing to a barrier-protective response in endothelial cells. Blood 110 (2007) 3909-3916
29. Bae J.S., Yang L., and Rezaie A.R. Receptors of the protein C activation and activated protein C signaling pathways are colocalized in lipid rafts of endothelial cells. Proc Natl Acad Sci U S A 104 (2007) 2867-2872
30. Joyce D.E., Chen Y., Erger R.A., Koretzky G.A., and Lentz S.R. Functional interactions between the thrombin receptor and the T-cell antigen receptor in human T-cell lines. Blood 90 (1997) 1893-1901
31. Lawrence T., Gilroy D.W., Colville-Nash P.R., and Willoughby D.A. Possible new role for NF-kappaB in the resolution of inflammation. Nat Med 7 (2001) 1291-1297
32. Joyce D.E., and Grinnell B.W. Recombinant human activated protein C attenuates the inflammatory response in endothelium and monocytes by modulating nuclear factor-kappaB. Crit Care Med 30 (2002) S288-S293
33. Menschikowski M., Hagelgans A., Heyne B., Hempel U., Neumeister V., Goez P., et al. Statins potentiate the IFN-gamma-induced upregulation of group IIA phospholipase A2 in human aortic smooth muscle cells and HepG2 hepatoma cells. Biochim Biophys Acta 1733 (2005) 157-171
34. Murakami M., Kudo I., and Inoue K. Molecular nature of phospholipases A2 involved in prostaglandin I2 synthesis in human umbilical vein endothelial cells. Possible participation of cytosolic and extracellular type II phospholipases A2. J Biol Chem 268 (1993) 839-844
35. Nakano T., Ohara O., Teraoka H., and Arita H. Group II phospholipase A2 mRNA synthesis is stimulated by two distinct mechanisms in rat vascular smooth muscle cells. FEBS Lett 261 (1990) 171-174
36. Kerr J.S., Stevens T.M., Davis G.L., McLaughlin J.A., and Harris R.R. Effects of recombinant interleukin-1 beta on phospholipase A2 activity, phospholipase A2 mRNA levels, and eicosanoid formation in rabbit chondrocytes. Biochem Biophys Res Commun 165 (1989) 1079-1084
37. Schalkwijk C., Pfeilschifter J., Marki F., and van den Bosch H. Interleukin-1 beta, tumor necrosis factor and forskolin stimulate the synthesis and secretion of group II phospholipase A2 in rat mesangial cells. Biochem Biophys Res Commun 174 (1991) 268-275
38. Oka S., and Arita H. Inflammatory factors stimulate expression of group II phospholipase A2 in rat cultured astrocytes. Two distinct pathways of the gene expression. J Biol Chem 266 (1991) 9956-9960
39. Crowl R.M., Stoller T.J., Conroy R.R., and Stoner C.R. Induction of phospholipase A2 gene expression in human hepatoma cells by mediators of the acute phase response. J Biol Chem 266 (1991) 2647-2651
40. Menschikowski M., Hagelgans A., Hempel U., Lattke P., Ismailov I., and Siegert G. On interaction of activated protein C with human aortic smooth muscle cells attenuating the secretory group IIA phospholipase A2 expression. Thromb Res 122 (2008) 69-76
41. Bae J.S., Yang L., Manithody C., and Rezaie A.R. 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 282 (2007) 9251-9259
42. Mosnier L.O., and Griffin J.H. Inhibition of staurosporine-induced apoptosis of endothelial cells by activated protein C requires protease-activated receptor-1 and endothelial cell protein C receptor. Biochem J 373 (2003) 65-70
43. Ossovskaya V.S., Bunnett N.W., de Garavilla L., Vergnolle N., Young S.H., Ennes H., et al. Protease-activated receptors: contribution to physiology and disease. Physiol Rev 84 (2004) 579-621
44. Bae J.S., Kim Y.U., Park M.K., and Rezaie A.R. Concentration dependent dual effect of thrombin in endothelial cells via Par-1 and Pi3 Kinase. J Cell Physiol 219 (2009) 744-751
45. Steinhoff M., Buddenkotte J., Shpacovitch V., Rattenholl A., Moormann C., Vergnolle N., et al. Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr Rev 26 (2005) 1-43
46. Shankar R., de la Motte C.A., Poptic E.J., and DiCorleto P.E. Thrombin receptor-activating peptides differentially stimulate platelet-derived growth factor production, monocytic cell adhesion, and E-selectin expression in human umbilical vein endothelial cells. J Biol Chem 269 (1994) 13936-13941
47. Feistritzer C., and Riewald M. Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine 1-phosphate receptor-1 crossactivation. Blood 105 (2005) 3178-3184
48. Alaoui-El-Azher M., Wu Y., Havet N., Israel A., Lilienbaum A., and Touqui L. Arachidonic acid differentially affects basal and lipopolysaccharide-induced sPLA(2)-IIA expression in alveolar macrophages through NF-kappaB and PPAR-gamma-dependent pathways. Mol Pharmacol 61 (2002) 786-794