Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin

Journal of Experimental Medicine

Volumn 197, Issue 11, 2003, Pages 1585-1598

  Falati, Shahrokh ^a   Liu, Qingde ^a,c   Gross, Peter ^a,e   Merrill Skoloff, Glenn ^a   Chou, Janet ^a   Vandendries, Erik ^a   Celi, Alessandro ^a   Croce, Kevin ^a,d   Furie, Barbara C ^a   Furie, Bruce ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Blood coagulation; Endothelium; Fibrin; Intravital microscopy; Thrombosis

Indexed keywords

CD14 ANTIGEN; FIBRIN; P SELECTIN GLYCOPROTEIN LIGAND 1; PADGEM PROTEIN; THROMBOPLASTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; ENDOTHELIUM INJURY; MICROCIRCULATION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; THROMBOCYTE ACTIVATION; THROMBOGENESIS; THROMBUS;

ANIMALS; ANTIGENS, CD14; BLOOD COAGULATION; ENDOTHELIUM, VASCULAR; LASERS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROCIRCULATION; MICROSCOPY, FLUORESCENCE; P-SELECTIN; THROMBOPLASTIN; THROMBOSIS;

EID: 12444303861     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20021868     Document Type: Article

References (54)

1. McEver, R.P. 1994. Selectins. Curr. Opin. Immunol. 6:75-84.
2. Kansas, G.S. 1996. Selectins and their ligands: current concepts and controversies. Blood. 88:3259-3287.
3. Yang, J., B.C. Furie, and B. Furie. 1999. The biology of P-selectin glycoprotein ligand-1: its role as a selectin counter-receptor in leukocyte-endothelial and leukocyte-platelet interaction. Thromb. Haemost. 81:1-7.
4. Hsu-Lin, S., C.L. Berman, B.C. Furie, D. August, and B. Furie. 1984. A platelet membrane protein expressed during platelet activation and secretion. Studies using a monoclonal antibody specific for thrombin-activated platelets. J. Biol. Chem. 259:9121-9126.
5. McEver, R.P., and M.N. Martin. 1984. A monoclonal antibody to a membrane glycoprotein binds only to activated platelets. J. Biol. Chem. 259:9799-9804.
6. Stenberg, P.E., R.P. McEver, M.A. Shuman, Y.V. Jacques, and D.F. Bainton. 1985. A platelet alpha-granule membrane protein (GMP-140) is expressed on the plasma membrane after activation. J. Cell Biol. 101:880-886.
7. Berman, C.L., E.L. Yeo, J.D. Wencel-Drake, B.C. Furie, M.H. Ginsberg, and B. Furie. 1986. A platelet alpha granule membrane protein that is associated with the plasma membrane after activation. Characterization and subcellular localization of platelet activation-dependent granule-external membrane protein. J. Clin. Invest. 78:130-137.
8. Larsen, E., A. Celi, G.E. Gilbert, B.C. Furie, J.K. Erban, R. Bonfanti, D.D. Wagner, and B. Furie. 1989. PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes. Cell. 59:305-312.
9. Sako, D., X.J. Chang, K.M. Barone, G. Vachino, H.M. White, G. Shaw, G.M. Veldman, K.M. Bean, T.J. Ahern, B. Furie, et al. 1993. Expression cloning of a functional glycoprotein ligand for P-selectin. Cell. 75:1179-1186.
10. Moore, K., N. Stults, S. Diaz, D. Smith, R. Cummings, A. Varki, and R. McEver. 1992. Identification of a specific glycoprotein ligand for P-selectin (CD62) on myeloid cells. J. Cell. Biol. 118:445-456.
11. Palabrica, T., R. Lobb, B.C. Furie, M. Aronovitz, C. Benjamin, Y.M. Hsu, S.A. Sajer, and B. Furie. 1992. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature. 359:848-851.
12. Celi, A., G. Pellegrini, R. Lorenzet, A. De Blasi, N. Ready, B.C. Furie, and B. Furie. 1994. P-selectin induces the expression of tissue factor on monocytes. Proc. Natl. Acad. Sci. USA. 91:8767-8771.
13. Furie, B., and B.C. Furie. 1988. The molecular basis of blood coagulation. Cell. 53:505-518.
14. Morrissey, J.H. 2001. Tissue factor: an enzyme cofactor and a true receptor. Thromb. Haemost. 86:66-74.
15. Morrissey, J.H., H. Fakhrai, and T.S. Edgington. 1987. Molecular cloning of the cDNA for tissue factor, the cellular receptor for the initiation of the coagulation protease cascade. Cell. 50:129-135.
16. Spicer, E.K., R. Horton, L. Bloem, R. Bach, K.R. Williams, A. Guha, J. Kraus, T.C. Lin, Y. Nemerson, and W.H. Konigsberg. 1987. Isolation of cDNA clones coding for human tissue factor: primary structure of the protein and cDNA. Proc. Natl. Acad. Sci. USA. 84:5148-5152.
17. Koyama, T., K. Nishida, S. Ohdama, M. Sawada, N. Murakami, S. Hirosawa, R. Kuriyama, K. Matsuzawa, R. Hasegawa, and N. Aoki. 1994. Determination of plasma tissue factor antigen and its clinical significance. Br. J. Haematol. 87:343-347.
18. Fareed, J., D.D. Callas, D. Hoppensteads, and E.W. Bermes. 1995. Tissue factor antigen levels in various biological fluids. Blood Coagul. Fibrinolysis. 6:S32-S36.
19. Zumbach, M., M. Hofmann, V. Borcea, T. Luther, M. Kotzsch, M. Muller, O. Hergesell, K. Andrassy, E. Ritz, R. Ziegler, et al. 1997. Tissue factor antigen is elevated in patients with microvascular complications of diabetes mellitus. Exp. Clin. Endocrinol. Diabetes. 105:206-212.
20. Giesen, P.L., U. Rauch, B. Bohrmann, D. Kling, M. Roque, J.T. Fallon, J.J. Badimon, J. Himber, M.A. Riederer, and Y. Nemerson. 1999. Blood-borne tissue factor: another view of thrombosis. Proc. Natl. Acad. Sci. USA. 96:2311-2315.
21. Rauch, U., D. Bonderman, B. Bohrmann, J.J. Badimon, J. Himber, M.A. Riederer, and Y. Nemerson. 2000. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood. 96:170-175.
22. Falati, S., P. Gross, G. Merrill-Skoloff, B.C. Furie, and B. Furie. 2002. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat. Med. 8:1175-1181.
23. Rosen, E.D., S. Raymond, A. Zollman, F. Noria, M. Sandoval-Cooper, A. Shulman, J.L. Merz, and F.J. Castellino. 2001. Laser-induced noninvasive vascular injury models in mice generate platelet- and coagulation-dependent thrombi. Am. J. Pathol. 158:1613-1622.
24. Yang, J., T. Hirata, K. Croce, G. Merrill-Skoloff, B. Tchernychev, E. Williams, R. Flaumenhaft, B.C. Furie, and B. Furie. 1999. Targeted gene disruption demonstrates that P-selectin glycoprotein ligand 1 (PSGL-1) is required for P-selectin-mediated but not E-selectin-mediated neutrophil rolling and migration. J. Exp. Med. 190:1769-1782.
25. Hirata, T., G. Merrill-Skoloff, M. Aab, J. Yang, B.C. Furie, and B. Furie. 2000. P-selectin glycoprotein ligand 1 (PSGL-1) is a physiological ligand for E-selectin in mediating T helper 1 lymphocyte migration. J. Exp. Med. 192:1669-1675.
26. Ley, K. 1995. Gene-targeted mice in leukocyte adhesion research. Microcirculation. 2:141-150.
27. 2-terminal region of fibrin. Mol. Immunol. 21:89-94.
28. Bristol, J.A., B.C. Furie, and B. Furie. 1993. Propeptide processing during factor IX biosynthesis. Effect of point mutations adjacent to the propeptide cleavage site. J. Biol. Chem. 268:7577-7584.
29. Dackiw, A.P., I.D. McGilvray, M. Woodside, A.B. Nathens, J.C. Marshall, and O.D. Rotstein. 1996. Prevention of endotoxin-induced mortality by antitissue factor immunization. Arch. Surg. 131:1273-1278.
30. Liu, Q., M.M. Rooney, A. Kasirer-Friede, E. Brown, S.T. Lord, and M.M. Frojmovic. 1998. Role of the gamma chain Ala-Gly-Asp-Val and Aα chain Arg-Gly-Asp-Ser sites of fibrinogen in coaggregation of platelets and fibrinogen-coated beads. Biochim. Biophys. Acta. 1385:33-42.
31. Lorenzet, R., J. Niemetz, A.J. Marcus, and M.J. Broekman. 1986. Enhancement of mononuclear procoagulant activity by platelet 12-hydroxyeicosatetraenoic acid. J. Clin. Invest. 78:418-423.
32. Andre, P., D. Hartwell, I. Hrachovinova, S. Saffaripour, and D.D. Wagner. 2000. Pro-coagulant state resulting from high levels of soluble P-selectin in blood. Proc. Natl. Acad. Sci. USA. 97:13835-13840.
33. Larsen, E., T. Palabrica, S. Sajer, G.E. Gilbert, D.D. Wagner, B.C. Furie, and B. Furie. 1990. PADGEM-dependent adhesion of platelets to monocytes and neutrophils is mediated by a lineage-specific carbohydrate, LNF III (CD15). Cell. 63:467-474.
34. Foxall, C., S.R. Watson, D. Dowbenko, C. Fennie, L.A. Lasky, M. Kiso, A. Hasegawa, D. Asa, and B.K. Brandley. 1992. The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. J. Cell Biol. 117:895-902.
35. Gross, P.L., B.C. Furie, and B. Furie. 2002. Kinetics of platelet activation, P-selectin expression and leukocyte rolling during arterial thrombus formation in vivo. Blood. 100:23a.
36. Yang, J., J. Galipeau, C.A. Kozak, B.C. Furie, and B. Furie. 1996. Mouse P-selectin glycoprotein ligand-1: molecular cloning, chromosomal localization, and expression of a functional P-selectin receptor. Blood. 87:4176-4186.
37. Semeraro, N., A. Biondi, R. Lorenzet, D. Locati, A. Mantovani, and M.B. Donati. 1983. Direct induction of tissue factor synthesis by endotoxin in human macrophages from diverse anatomical sites. Immunology. 50:529-535.
38. Xia, L., M. Sperandio, T. Yago, J.M. McDaniel, R.D. Cummings, S. Pearson-White, K. Ley, and R.P. McEver. 2002. P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J. Clin. Invest. 109:939-950.
39. Subramaniam, M., P.S. Frenette, S. Saffaripour, R.C. Johnson, R.O. Hynes, and D.D. Wagner. 1996. Defects in hemostasis in P-selectin-deficient mice. Blood. 87:1238-1242.
40. Ruggeri, Z., M. Subramanian, J. Dent, D. Wagner, and E. Saldivar. 2000. P-Selectin and the three dimensional structure of platelet thrombi. Blood. 96(Suppl. 1):812a.
41. Muller, I., A. Zillman, M. Kotzsch, M. Spannagl, S. Zahler, T. Luter, and B. Engelmann. 2001. Collagen stimulation triggers the rapid activation of platelet-associated tissue factor. Thrombosis and Haemostasis Supplement July. 201:P2887.
42. Nieuwland, R., R.J. Berckmans, S. McGregor, A.N. Boing, F.P. Romijn, R.G. Westendorp, C.E. Hack, and A. Sturk. 2000. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood. 95:930-935.
43. Sims, P.J., T. Wiedmer, C.T. Esmon, H.J. Weiss, and S.J. Shattil. 1989. Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane: studies in Scott syndrome: an isolated defect in platelet procoagulant activity. J. Biol. Chem. 254:17049-17057.
44. Thiagarajan, P., and J.F. Tait. 1991. Collagen-induced exposure of anionic phospholipid in platelets and platelet-derived microparticles. J. Biol. Chem. 266:24302-24307.
45. Siljander, P., O. Carpen, and R. Lassila. 1996. Platelet-derived microparticles associate with fibrin during thrombosis. Blood. 87:4651-4663.
46. Satta, N., F. Toti, O. Feugeas, A. Bohbot, J. Dachary-Prigent, V. Eschwege, H. Hedman, and J.M. Freyssinet. 1994. Monocyte vesiculation is a possible mechanism for dissemination of membrane-associated procoagulant activities and adhesion molecules after stimulation by lipopolysaccharide. J. Immunol. 153:3245-3255.
47. Berckmans, R.J., R. Nieuwland, A.N. Boing, F.R.H.T.M. Romijn, C.E. Hack, and A. Sturk. 2001. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb. Haemost. 85:639-646.
48. Mesri, M., and D.C. Altieri. 1999. Leukocyte microparticles stimulate endothelial cell cytokine release and tissue factor induction in a JNK1 signaling pathway. J. Biol. Chem. 274:23111-23118.
49. Combes, V., A.-C. Simon, G.-E. Grau, D. Arnoux, L. Camoin, F. Sabatier, M. Mutin, M. Sanmarco, J. Sampol, and F. Dignat-George. 1999. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J. Clin. Invest. 104:93-102.
50. Sabatier, F., V. Roux, F. Anfosso, L. Camoin, J. Sampol, and F. Dignat-George. 2002. Interaction of endothelial microparticles with monocytic cells in vitro induces tissue factor-dependent procoagulant activity. Blood. 99:3962-3970.
51. Schecter, A.D., B. Spirn, M. Rossikhina, P.L. Giesen, V. Bogdanov, J.T. Fallon, E.A. Fisher, L.M. Schnapp, Y. Nemerson, and M.B. Taubman. 2000. Release of active tissue factor by human arterial smooth muscle cells. Circ. Res. 87:126-132.
52. Gilbert, G.E., P.J. Sims, T. Wiedmer, B. Furie, B.C. Furie, and S.J. Shattil. 1991. Platelet-derived microparticles express high affinity receptors for factor VIII. J. Biol. Chem. 266:17261-17268.
53. Le, D.T., S.I. Rapaport, and L.V. Rao. 1992. Relations between factor VIIa binding and expression of factor VIIa/tissue factor catalytic activity on cell surfaces. J. Biol. Chem. 267:15447-15454.
54. Mayadas, T.N., R.C. Johnson, H. Rayburn, R.O. Hynes, and D.D. Wagner. 1993. Leukocyte rolling and extravasation are severely compromised in P-selectin-deficient mice. Cell. 74:541-554.