Cytofluorometric Identification of Plasmin-Sensitive Factor XIIIa Binding to Platelets

Julie A Kreager; Dana V Devine; Charles S Greenberg

doi:10.1055/s-0038-1647641

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 1988; 60(01): 088-093
DOI: 10.1055/s-0038-1647641

Original Article

Schattauer GmbH Stuttgart

Cytofluorometric Identification of Plasmin-Sensitive Factor XIIIa Binding to Platelets

Julie A Kreager

^*The Division of Hematology-Oncology, Department of Medicine, Duke University Medical Center, Durham, NC, USA

,

Dana V Devine

^*The Division of Hematology-Oncology, Department of Medicine, Duke University Medical Center, Durham, NC, USA

,

Charles S Greenberg

^**The Department of Pathology, Duke University Medical Center, Durham, NC, USA

› Author Affiliations

Abstract

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Summary

We have investigated the binding of blood coagulation factor XIIIa to thrombin-stimulated platelets using cytofluorometric analysis. Washed thrombin-stimulated platelets bound exoge-nously added factor XIIIa in a calcium-dependent reaction. The expression of endogenous platelet factor XIII was also detected on the surface of thrombin-stimulated platelets. When fluorescence analysis was performed based on particle size, factor XIIIa bound to the surface of greater than 95% of particles which contained more than one platelet, but only 50% of single platelets. The binding of factor XIIIa to thrombin-stimulated platelets was inhibited by plasmin. Plasmin also inhibited thrombin-dependent expression of the factor XIIIa binding site on platelets. Experiments in which thrombin-stimulated platelets were incubated with factor XIIIa in the presence of ¹²⁵I-dimethyl-casein or ³H-putrescine demonstrated that platelets bear both glutamyl and lysyl substrates for factor XIIIa. Thrombin increased the expression of factor XIIIa substrates by platelets. Plasmin inhibited both the expression of factor XIIIa substrates and degraded them. The binding of factor XIIIa to thrombin-stimulated platelets and the availability of factor XIIIa substrates on the platelet surface could provide a mechanism by which factor XIIIa stabilizes the hemostatic plug by promoting crosslinking reactions between platelet membrane proteins and adhesive glycoproteins. In contrast, plasmin inhibition of factor XIIIa binding and crosslinking could disrupt hemostasis.

Key words

Factor XIII - Platelets - Plasmin

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References

References
1 Bennett JS, Vilare G. Exposure of platelet fibrinogen receptors by ADP and epinephrine. J Clin Invest 1979; 64: 1393-1397
2 Greengard JS, Griffin JH. Receptors for high molecular weight kininogen on stimulated washed human platelets. Biochemistry 1985; 23: 6863-6866
3 Mitchell CA, Salem HH. Cleavage of protein S by a platelet membrane protease. J Clin Invest 1987; 79: 374-378
4 Lipscomb MS, Walsh PN. Human platelets and factor XI. J Clin Invest 1979; 63: 1006-1112
5 Miletich JP, Jackson CM, Majerus PW. Properties of the factor Xa binding sites on human platelets. J Biol Chem 1978; 253: 6908-6913
6 Kane WH, Majerus PW. The interaction of human coagulation factor Va with platelets. J Biol Chem 1982; 257: 3963-3968
7 Folk JE, Finlayson JS. The epsilon (γ-glutamyl) lysine crosslink and the catalytic role of transglutaminase. Adv Protein Chem 1977; 31: 1-49
8 Sakata Y, Aoki N. Cross-linking of α₂-plasmin inhibitor to fibrin by fibrin-stabilizing factor. J Clin Invest 1980; 65: 290-294
9 Lopaciuk S, Lovette KM, McDonagh J, Chuang HYK, McDonagh RP. Subcellular distribution of fibrinogen and factor XIII in platelets. Thromb Res 1976; 8: 453-460
10 Joist JH, Niewiarowski S. Retention of platelet fibrin-stabilizing factor during the platelet release reaction and clot retraction. Thromb Diath Haemorrh 1973; 29: 679-684
11 McDonagh J, McDonagh RP. Factor XIII from human platelets: Effect on fibrin crosslinking. Thromb Res 1972; 1: 147-153
12 Cohen I, Glaser T, Veis A, Bruner-Lorand J. Ca²⁺-dependent crosslinking process in human platelets. Biochim Biophys Acta 1981; 676: 137-144
13 Cohen I, Gerrard JM, White JG. Ultrastructure of clots during isometric contraction. J Cell Biol 1982; 93: 775-782
14 Wang DL, Huh MM, Colman RW. Human factor V is crosslinked to actin by factor XIIIa. Fed Proc 1987; 46: 422
15 Saito Y, Imada T, Takagi J, Kikuchi T, Inada Y. Platelet factor XIII: The collagen receptor. J Biol Chem 1986; 261: 1355-1358
16 Plow EF, Ginsberg MH. Specific and saturable binding of plasma fibronectin to thrombin-stimulated human platelets. J Biol Chem 1981; 256: 9477-9480
17 Phillips DR, Jennings LK, Prasanna HR. Ca²⁺-mediated association of glycoprotein G with human platelets. J Biol Chem 1980; 255: 11629-11631
18 Kao KJ, Pizzo SV, McKee PA. Demonstration and characterization of specific binding sites for factor VIII/von Willebrand factor on human platelets. J Clin Invest 1979; 63: 656-660
19 Mosher DF. Crosslinking of cold-insoluble globulin by fibrin stabilizing factor. J Biol Chem 1975; 250: 6614-6619
20 Bale MD, Mosher DF. Thrombospondin is a substrate for blood coagulation factor XIIIa. Biochemistry 1986; 25: 5667-5671
21 Bockenstead P, McDonagh J, Handin RI. Binding and covalent crosslinking of purified von Willebrand factor to native monomeric collagen. J Clin Invest 1986; 78: 551-557
22 Greenberg CS, Shuman MA. Specific binding of blood coagulation factor XIIIa thrombin-stimulated platelets. J Biol Chem 1984; 259: 14721-14726
23 Schwartz ML, Pizzo SV, Hill RL, McKee PA. Human factor XIII from plasma and platelets. J Biol Chem 1973; 246: 5851-5856
24 Chung SI, Lewis MS, Folk JE. Relationships of the catalytic properties of human plasma and platelet transglutaminases (activated blood coagulation factor XIII) to their subunit structures. J Biol Chem 1974; 249: 940-945
25 Greenberg CS, Achyuthan KE, Fenton JW. Factor XIIIa formation promoted by complexing of α-thrombin, fibrin, and plasma factor XIII. Blood 1987; 69: 867-872
26 Rosse WF, Devine DV, Ware R. The reactions of IgG-binding ligands with platelet and platelet associated IgG. J Clin Invest 1984; 73: 489-493
27 Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 1979; 76: 4350-4355
28 Miraglia C, Greenberg CS. Measurement of blood coagulation factor XIIIa formation in plasma containing glycyl-L-prolyl-L-arginyl-L-proline. Anal Biochem 1985; 144: 165-172
29 Adelman B, Michelson AD, Handin RI, Ault KA. Evaluation of platelet glycoprotein lb by fluorescence flow cytometry. Blood 1985; 66: 423-429
30 Jennings LK, Ashmun RA, Wang WC, Dockter ME. Analysis of platelet glycoprotein IIb-IIIa and Glanzmann’s thrombasthenia in whole blood by flow cytometry. Blood 1986; 68: 173-178
31 Kasahara K, Takagi J, Sekiya F, Inada Y, Saito Y. Analysis of distribution of receptors among platelets by flow cytometry. Thromb Res 1987; 45: 763-769
32 Kradin DM, Lynch GW, Kurnick JT, Erikson M, Colvin RB, McDonagh J. Factor XIIIa is synthesized and expressed on the surface of U937 cells and alveolar macrophages. Blood 1987; 69: 778-782
33 Mosher DF. Cross-linking of cold insoluble globulin by fibrin-stabilizing factor. J Biol Chem 1975; 250: 6614-6619
34 Kreager JA, Devine DV, Greenberg CS. Thrombin stimulated platelets provide substrates and binding sites for factor XIIIa to stabilize the hemostatic plug. Blood 1986; 68: 320a
35 Messmore HL, Walenga JM, Fareed J. Molecular markers of platelet activation. Semin Thromb Hemostas 1984; 10: 264-269
36 Schafer AI, Adelman B. Plasmin inhibition of platelet function and arachidonic acid metabolism. J Clin Invest 1985; 75: 456-462
37 Adelman B, Michelson AD, Loscalzo J, Greenberg J, Handin RI. Plasmin effect on platelet glycoprotein Ib-von Willebrand factor interactions. Blood 1985; 65: 32-39
38 Rider DM, McDonagh J. Resistance of factor XIII to degradation or activation by plasmin. Biochim Biophys Acta 1981; 675: 171-177