Download PDF
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
Further Information

Publication History

Received 06 July 1987

Accepted after revision 20 April 1988

Publication Date:
30 June 2018 (online)

  PDF Download  Permissions and Reprints

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
 

  • References

  • 1 Bennett JS, Vilare G. Exposure of platelet fibrinogen receptors by ADP and epinephrine. J Clin Invest 1979; 64: 1393-1397
    CrossrefPubMedGoogle Scholar
  • 2 Greengard JS, Griffin JH. Receptors for high molecular weight kininogen on stimulated washed human platelets. Biochemistry 1985; 23: 6863-6866
    PubMedGoogle Scholar
  • 3 Mitchell CA, Salem HH. Cleavage of protein S by a platelet membrane protease. J Clin Invest 1987; 79: 374-378
    CrossrefPubMedGoogle Scholar
  • 4 Lipscomb MS, Walsh PN. Human platelets and factor XI. J Clin Invest 1979; 63: 1006-1112
    CrossrefPubMedGoogle Scholar
  • 5 Miletich JP, Jackson CM, Majerus PW. Properties of the factor Xa binding sites on human platelets. J Biol Chem 1978; 253: 6908-6913
    PubMedGoogle Scholar
  • 6 Kane WH, Majerus PW. The interaction of human coagulation factor Va with platelets. J Biol Chem 1982; 257: 3963-3968
    PubMedGoogle Scholar
  • 7 Folk JE, Finlayson JS. The epsilon (γ-glutamyl) lysine crosslink and the catalytic role of transglutaminase. Adv Protein Chem 1977; 31: 1-49
    PubMedGoogle Scholar
  • 8 Sakata Y, Aoki N. Cross-linking of α2-plasmin inhibitor to fibrin by fibrin-stabilizing factor. J Clin Invest 1980; 65: 290-294
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 11 McDonagh J, McDonagh RP. Factor XIII from human platelets: Effect on fibrin crosslinking. Thromb Res 1972; 1: 147-153
    CrossrefPubMedGoogle Scholar
  • 12 Cohen I, Glaser T, Veis A, Bruner-Lorand J. Ca2+-dependent crosslinking process in human platelets. Biochim Biophys Acta 1981; 676: 137-144
    CrossrefPubMedGoogle Scholar
  • 13 Cohen I, Gerrard JM, White JG. Ultrastructure of clots during isometric contraction. J Cell Biol 1982; 93: 775-782
    CrossrefPubMedGoogle Scholar
  • 14 Wang DL, Huh MM, Colman RW. Human factor V is crosslinked to actin by factor XIIIa. Fed Proc 1987; 46: 422
    PubMedGoogle Scholar
  • 15 Saito Y, Imada T, Takagi J, Kikuchi T, Inada Y. Platelet factor XIII: The collagen receptor. J Biol Chem 1986; 261: 1355-1358
    PubMedGoogle Scholar
  • 16 Plow EF, Ginsberg MH. Specific and saturable binding of plasma fibronectin to thrombin-stimulated human platelets. J Biol Chem 1981; 256: 9477-9480
    PubMedGoogle Scholar
  • 17 Phillips DR, Jennings LK, Prasanna HR. Ca2+-mediated association of glycoprotein G with human platelets. J Biol Chem 1980; 255: 11629-11631
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 19 Mosher DF. Crosslinking of cold-insoluble globulin by fibrin stabilizing factor. J Biol Chem 1975; 250: 6614-6619
    PubMedGoogle Scholar
  • 20 Bale MD, Mosher DF. Thrombospondin is a substrate for blood coagulation factor XIIIa. Biochemistry 1986; 25: 5667-5671
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 22 Greenberg CS, Shuman MA. Specific binding of blood coagulation factor XIIIa thrombin-stimulated platelets. J Biol Chem 1984; 259: 14721-14726
    PubMedGoogle Scholar
  • 23 Schwartz ML, Pizzo SV, Hill RL, McKee PA. Human factor XIII from plasma and platelets. J Biol Chem 1973; 246: 5851-5856
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 29 Adelman B, Michelson AD, Handin RI, Ault KA. Evaluation of platelet glycoprotein lb by fluorescence flow cytometry. Blood 1985; 66: 423-429
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 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
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 33 Mosher DF. Cross-linking of cold insoluble globulin by fibrin-stabilizing factor. J Biol Chem 1975; 250: 6614-6619
    PubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 35 Messmore HL, Walenga JM, Fareed J. Molecular markers of platelet activation. Semin Thromb Hemostas 1984; 10: 264-269
    Article in Thieme ConnectPubMedGoogle Scholar
  • 36 Schafer AI, Adelman B. Plasmin inhibition of platelet function and arachidonic acid metabolism. J Clin Invest 1985; 75: 456-462
    CrossrefPubMedGoogle Scholar
  • 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
    PubMedGoogle Scholar
  • 38 Rider DM, McDonagh J. Resistance of factor XIII to degradation or activation by plasmin. Biochim Biophys Acta 1981; 675: 171-177
    CrossrefPubMedGoogle Scholar