Lactadherin blocks thrombosis and hemostasis in vivo: Correlation with platelet phosphatidylserine exposure

Journal of Thrombosis and Haemostasis

Volumn 6, Issue 7, 2008, Pages 1167-1174

  Shi, J ^a   Pipe, S W ^b   Rasmussen, J T ^c   Heegaard, C W ^c   Gilbert, Gary E ^a,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c AARHUS UNIVERSITY   (Denmark)

^d VA BOSTON HEALTHCARE SYSTEM   (United States)

Author keywords

Annexin; Factor V; Factor VIII; Lactadherin; Phosphatidylserine; Platelets

Indexed keywords

BLOOD CLOTTING FACTOR 10A; CALCIUM ION; FERRIC CHLORIDE; LACTADHERIN; LIPOCORTIN 5; PHOSPHATIDYLSERINE; THROMBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL MEMBRANE; BINDING SITE; BLEEDING TIME; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEMOSTASIS; IN VIVO STUDY; MESENTERIC VEIN THROMBOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION;

ANIMALS; ANNEXIN A5; ANTIGENS, SURFACE; BINDING SITES; BLOOD PLATELETS; CAROTID ARTERY DISEASES; CYSTEINE ENDOPEPTIDASES; HEMOSTASIS; MESENTERIC VEINS; MICE; MILK PROTEINS; NEOPLASM PROTEINS; PHOSPHATIDYLSERINES; THROMBOPLASTIN; THROMBOSIS;

EID: 45549085611     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2008.03010.x     Document Type: Article

References (43)

1. Alberio L, Safa O, Clemetson KJ, Esmon CT, Dale GL. Surface expression and functional characterization of alpha-granule factor V in human platelets: Effects of ionophore A23187, thrombin, collagen, and convulxin. Blood 2000; 95: 1694-702.
2. Cohen Z, Wilson J, Ritter L, McDonagh P. Caspase inhibition decreases both platelet phosphatidylserine exposure and aggregation: Caspase inhibition of platelets. Thromb Res 2004; 113: 387-93.
3. London FS, Marcinkiewicz M, Walsh PN. A subpopulation of platelets responds to thrombin- or SFLLRN-stimulation with binding sites for factor IXa. J Biol Chem 2004; 279: 19854-9.
4. Bevers E, Comfurius P, Van Rijn J, Hemker H, Zwaal R. Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem 1982; 122: 429-36.
5. Williamson P, Bevers EM, Smeets EF, Comfurius P, Schlegel RA, Zwaal RFA. Continuous analysis of the mechanism of activated transbilayer lipid movement in platelets. Biochemistry 1995; 34: 10448-55.
6. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. Annexin V for flow cytometric detection of phosphatidylserine expression on B.cells undergoing apoptosis. Blood 1994; 84: 1415-20.
7. Phillips JE, Lord ST, Gilbert GE. Fibrin stimulates platelets to increase factor VIIIa binding site expression. J Thromb Haemost 2004; 2: 1806-15.
8. Ahmad SS, Rawala-Sheikh R, Ashby B, Walsh PN. Platelet receptor-mediated factor X activation by factor IXa: High-affinity factor IXa receptors induced by factor VIII are deficient on platelets in Scott syndrome. J Clin Invest 1989; 84: 824-8.
9. Stubbs J, Lekutis C, Singer K, Bui A, Yuzuki D, Srinivasan U, Parry G. cDNA cloning of a mouse mammary epithelial cell surface protein reveals the existence of epidemal growth factor-like domains linked to factor VIII-like sequences. Proc Natl Acad Sci USA 1990; 87: 8417-21.
10. Andersen MH, Graversen H, Fedosov SN, Petersen TE, Rasmussen JT. Functional analyses of two cellular binding domains of bovine lactadherin. Biochemistry 2000; 39: 6200-6.
11. Shi J, Heegaard CW, Rasmussen JT, Gilbert GE. Lactadherin binds selectively to membranes containing phosphatidyl-L-serine and increased curvature. Biochim Biophys Acta 2004; 1667: 82-90.
12. Shi J, Gilbert GE. Lactadherin inhibits enzyme complexes of blood coagulation by competing for phospholipid binding sites. Blood 2003; 101: 2628-36.
13. Shi J, Shi Y, Waehrens LN, Rasmussen JT, Heegaard CW, Gilbert GE. Lactadherin detects early phosphatidylserine exposure on immortalized leukemia cells undergoing programmed cell death. Cytometry A 2006; 69: 1193-201.
14. Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, Grinstein S. Membrane phosphatidylserine regulates surface charge and protein localization. Science 2008; 319: 210-13.
15. Gilbert GE, Drinkwater D, Barter S, Clouse SB. Specificity of phosphatidylserine-containing membrane binding sites for factor VIII: studies with model membranes supported by glass microspheres (Lipospheres). J Biol Chem 1992; 267: 15861-8.
16. Moore EW. Ionized calcium in normal serum, ultrafiltrates, and whole blood determined by ion-exchange electrodes. J Clin Invest 1970; 49: 318-34.
17. Gemmell CH, Sefton MV, Yeo EL. Platelet-derived microparticle formation involves glycoprotein-IIb-IIIa - inhibition by RGDS and a Glanzmann's thrombasthenia defect. J Biol Chem 1993; 268: 14586-9.
18. Phillips JE, Gilbert GE. Platelet exposure of functional factor VIII binding sites requires stimulation by thrombin and shear stress. Blood 1995; 86: 549a.
19. Shi J, Gilbert GE, Kokubo Y, Ohashi T. Role of the liver in regulating numbers of circulating neutrophils. Blood 2001; 98: 1226-30.
20. Eitzman DT, Westrick RJ, Nabel EG, Ginsburg D. Plasminogen activator inhibitor-1 and vitronectin promote vascular thrombosis in mice. Blood 2000; 95: 577-80.
21. Gilbert GE, Drinkwater D. Specific membrane binding of factor VIII is mediated by O-phospho-L-serine, a moiety of phosphatidylserine. Biochemistry 1993; 32: 9577-85.
22. Comfurius P, Smeets EF, Willems GM, Bevers EM, Zwaal RFA. Assembly of the prothrombinase complex on lipid vesicles depends on the stereochemical configuration of the polar headgroup of phosphatidylserine. Biochemistry 1994; 33: 10319-24.
23. Gilbert GE, Arena AA. Activation of the factor VIIIa-factor IXa enzyme complex of blood coagulation by membranes containing phosphatidyl-L-serine. J Biol Chem 1996; 271: 11120-5.
24. Gilbert GE, Arena AA. Partial activation of the factor VIIIa-factor IXa enzyme complex by dihexanoic phosphatidylserine at submicellar concentrations. Biochemistry 1997; 36: 10768-76.
25. Shao C, Novakovic VA, Head JF, Seaton BA, Gilbert GE. Crystal structure of lactadherin C2 domain at 1.7 angstrom resolution with mutational and computational analyses of its membrane-binding motif. J Biol Chem 2007; 283: 7230-41.
26. Munnix IC, Strehl A, Kuijpers MJ, Auger JM, van der Meijden PE, van Zandvoort MA, oude Egbrink MG, Nieswandt B, Heemskerk JW. The glycoprotein VI-phospholipase Cgamma2 signaling pathway controls thrombus formation induced by collagen and tissue factor in vitro and in vivo. Arterioscler Thromb Vasc Biol 2005; 25: 2673-8.
27. Pauer HU, Baird TR, Johnston K, Seaton BA, Furie B, Furie BC. Prothrombin fragment 1 and annexin V localize differently after laser induced vascular injury in vivo. J Thromb Haemost 2005; 3: Abstract OR374.
28. Andree H, Reutelingsperger C, Hauptmann R, Hemker H, Hermens W, Willems G. Binding of vascular anticoagulant α (VACα) to planar phospholipid bilayers. J Biol Chem 1990; 265: 4923-8.
29. Dachary-Prigent J, Freyssinet JM, Pasquet JM, Carron JC, Nurden AT. Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: A flow cytometry study showing a role for free sulfhydryl groups. Blood 1993; 81: 2554-65.
30. Reutelingsperger CPM, Hornstra G, Hemker HC. Isolation and partial purification of a novel anticoagulant from arteries of human umbilical cord. Eur J Biochem 1985; 151: 625-9.
31. Tait JF, Sakata MS, McMullen BA, Miao CH, Funakoshi T, Hendrickson LE, Fujikawa K. Placental anticoagulant proteins: Isolation and comparative characterization of four members of the lipocortin family. Biochemistry 1988; 27: 6268-76.
32. London F, Ahmad SS, Walsh PN. Annexin V inhibition of factor IXa-catalyzed factor X activation on human platelets and on negatively-charged phospholipid vesicles. Biochemistry 1996; 35: 16886-97.
33. Dasgupta SK, Guchhait P, Thiagarajan P. Lactadherin binding and phosphatidylserine expression on cell surface - comparison with annexin A5. Transl Res 2006; 148: 19-25.
34. Romisch J, Seiffge D, Reiner G, Paques EP, Heimburger N. In-vivo antithrombotic potency of placenta protein 4 (annexin V). Thromb Res 1991; 61: 93-104.
35. Van Ryn-McKenna J, Merk H, Muller TH, Buchanan MR, Eisert WG. The effects of heparin and annexin V on fibrin accretion after injury in the jugular veins of rabbits. Thromb Haemost 1993; 69: 227-30.
36. Thiagarajan P, Benedict CR. Inhibition of arterial thrombosis by recombinant annexin V in a rabbit carotid artery injury model. Circulation 1997; 96: 2339-47.
37. Tracy P, Peterson J, Nesheim M, McDuffie F, Mann K. Interaction of coagulation factor V and factor Va with platelets. J Biol Chem 1979; 254: 10354-61.
38. Swords NA, Tracy PB, Mann KG. Intact platelet membranes, not platelet-released microvesicles, support the procoagulant activity of adherent platelets. Arterioscler Thromb 1993; 13: 1613-22.
39. George J, Thoi L, McManus L, Reimann T. Isolation of human platelet membrane microparticles from plasma and serum. Blood 1982; 60: 834-40.
40. Gilbert GE, Sims PJ, Wiedmer T, Furie B, Furie BC, Shattil SJ. Platelet-derived microparticles express high affinity receptors for factor VIII. J Biol Chem 1991; 266: 17261-8.
41. Bevers E, Wiedmer T, Comfurius P, Shattil S, Weiss H, Zwaal R, Sims P. Defective Ca2+-induced microvesiculation and deficient expression of procoagulant activity in erythrocytes from a patient with a bleeding disorder: A study of the red blood cells of Scott syndrome. Blood 1992; 79: 380-8.
42. Kempton CL, Hoffman M, Roberts HR, Monroe DM. Platelet heterogeneity: variation in coagulation complexes on platelet subpopulations. Arterioscler Thromb Vasc Biol 2005; 25: 861-6.
43. Jobe SM, Wilson KM, Leo L, Raimondi A, Molkentin JD, Lentz SR, Di Paola J. Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood 2008; 111: 1257-65.